Physical Gold Nanoparticle-Decorated Polyethylene Glycol-Hydroxyapatite Composites Guide Osteogenesis and Angiogenesis of Mesenchymal Stem Cells
Abstract
:1. Introduction
2. Materials and Methods
2.1. Material Preparation
2.1.1. Preparation of Polyethylene Glycol (PEG) Stock Solution
2.1.2. Preparation of Polyethylene Glycol-Hydroxyapatite (HA)
2.1.3. Preparation of Polyethylene Glycol-Hydroxyapatite-Gold Nanoparticles (PEG-HA-AuNPs)
2.1.4. Preparation of Surface Coatings
2.2. Material Characterization
2.2.1. Fourier Transform Infrared Spectroscopy (FTIR) Analysis
2.2.2. Surface-Enhanced Raman Scattering
2.2.3. UV–Visible Spectroscopy
2.2.4. Atomic Force Microscopy (AFM)
2.2.5. X-ray Photoelectron Spectroscopy (XPS)
2.2.6. Free Radical Scavenging Ability
2.3. Biocompatibility Test
2.3.1. Cell Culture Condition
2.3.2. MTT Assay
2.3.3. Reactive Oxygen Species (ROS) Generation Analysis
2.3.4. Actin Fiber Fluorescent Staining
2.3.5. Cell Morphology and Adhesion Ability
2.3.6. Monocyte Activation Test
2.3.7. Platelet Activation Test
2.4. Biological Functional Assay
2.4.1. Cell Migration Assay
2.4.2. Gelatin Zymography Analysis
2.4.3. Enzyme-Linked Immunosorbent Assay
2.4.4. Real-Time PCR Assay
2.4.5. Alizarin Red S Staining (ARS)
2.5. Rat Subcutaneous Implantation
2.6. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Zhu, T.; Cui, Y.; Zhang, M.; Zhao, D.; Liu, G.; Ding, J. Engineered three-dimensional scaffolds for enhanced bone regeneration in osteonecrosis. Bioact. Mater. 2020, 5, 584–601. [Google Scholar] [CrossRef] [PubMed]
- Zhao, D.; Zhu, T.; Li, J.; Cui, L.; Zhang, Z.; Zhuang, X.; Ding, J. Poly (lactic-co-glycolic acid)-based composite bone-substitute materials. Bioact. Mater. 2021, 6, 346–360. [Google Scholar] [CrossRef] [PubMed]
- Qiu, H.; Guo, H.; Li, D.; Hou, Y.; Kuang, T.; Ding, J. Intravesical Hydrogels as Drug Reservoirs. Trends Biotechnol. 2020, 38, 579–583. [Google Scholar] [CrossRef] [PubMed]
- Le, H.; Xu, W.; Zhuang, X.; Chang, F.; Wang, Y.; Ding, J. Mesenchymal stem cells for cartilage regeneration. J. Tissue Eng. 2020, 11, 2041731420943839. [Google Scholar] [CrossRef]
- Cui, L.; Zhang, J.; Zou, J.; Yang, X.; Guo, H.; Tian, H.; Zhang, P.; Wang, Y.; Zhang, N.; Zhuang, X.; et al. Electroactive composite scaffold with locally expressed osteoinductive factor for synergistic bone repair upon electrical stimulation. Biomaterials 2020, 230, 119617. [Google Scholar] [CrossRef]
- Kim, S.S.; Sun Park, M.; Jeon, O.; Yong Choi, C.; Kim, B.S. Poly(lactide-co-glycolide)/hydroxyapatite composite scaffolds for bone tissue engineering. Biomaterials 2006, 27, 1399–1409. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Zheng, Q.; Guo, X.; Zou, Z.; Liu, Y.; Lan, S.; Chen, L.; Deng, Y. Bone induction by surface-double-modified true bone ceramics in vitro and in vivo. Biomed. Mater. 2013, 8, 035005. [Google Scholar] [CrossRef] [PubMed]
- Garai, S.; Sinha, A. Biomimetic nanocomposites of carboxymethyl cellulose-hydroxyapatite: Novel three dimensional load bearing bone grafts. Colloids Surf. B Biointerfaces 2014, 115, 182–190. [Google Scholar] [CrossRef]
- Moore, W.R.; Graves, S.E.; Bain, G.I. Synthetic bone graft substitutes. ANZ J. Surg. 2001, 71, 354–361. [Google Scholar] [CrossRef]
- Wahl, D.A.; Czernuszka, J.T. Collagen-hydroxyapatite composites for hard tissue repair. Eur. Cell Mater. 2006, 11, 43–56. [Google Scholar] [CrossRef]
- Di Toro, R.; Betti, V.; Spampinato, S. Biocompatibility and integrin-mediated adhesion of human osteoblasts to poly(DL-lactide-co-glycolide) copolymers. Eur. J. Pharm. Sci. 2004, 21, 161–169. [Google Scholar] [CrossRef]
- Wang, G.; Liu, S.J.; Ueng, S.W.; Chan, E.C. The release of cefazolin and gentamicin from biodegradable PLA/PGA beads. Int. J. Pharm. 2004, 273, 203–212. [Google Scholar] [CrossRef] [PubMed]
- Clèries, L.; Fernández-Pradas, J.M.; Morenza, J.L. Behavior in simulated body fluid of calcium phosphate coatings obtained by laser ablation. Biomaterials 2000, 21, 1861–1865. [Google Scholar] [CrossRef]
- Ramesh, N.; Moratti, S.C.; Dias, G.J. Hydroxyapatite-polymer biocomposites for bone regeneration: A review of current trends. J. Biomed. Mater. Res. B Appl. Biomater. 2018, 106, 2046–2057. [Google Scholar] [CrossRef]
- Webster, T.J.; Ergun, C.; Doremus, R.H.; Siegel, R.W.; Bizios, R. Specific proteins mediate enhanced osteoblast adhesion on nanophase ceramics. J. Biomed. Mater. Res. 2000, 51, 475–483. [Google Scholar] [CrossRef]
- Murugan, R.; Ramakrishna, S. Development of nanocomposites for bone grafting. Compos. Sci. Technol. 2005, 65, 2385–2406. [Google Scholar] [CrossRef]
- Costa-Rodrigues, J.; Carmo, S.; Perpétuo, I.P.; Monteiro, F.J.; Fernandes, M.H. Osteoclastogenic differentiation of human precursor cells over micro- and nanostructured hydroxyapatite topography. Biochim. Biophys. Acta 2016, 1860, 825–835. [Google Scholar] [CrossRef]
- Wang, P.; Yu, T.; Lv, Q.; Li, S.; Ma, X.; Yang, G.; Xu, D.; Liu, X.; Wang, G.; Chen, Z.; et al. Fabrication of hydroxyapatite/hydrophilic graphene composites and their modulation to cell behavior toward bone reconstruction engineering. Colloids Surf. B Biointerfaces 2019, 173, 512–520. [Google Scholar] [CrossRef]
- Zheng, P.; Hu, X.; Lou, Y.; Tang, K. A Rabbit Model of Osteochondral Regeneration Using Three-Dimensional Printed Polycaprolactone-Hydroxyapatite Scaffolds Coated with Umbilical Cord Blood Mesenchymal Stem Cells and Chondrocytes. Med. Sci. Monit. 2019, 25, 7361–7369. [Google Scholar] [CrossRef]
- Jeong, S.I.; Ko, E.K.; Yum, J.; Jung, C.H.; Lee, Y.M.; Shin, H. Nanofibrous poly(lactic acid)/hydroxyapatite composite scaffolds for guided tissue regeneration. Macromol. Biosci 2008, 8, 328–338. [Google Scholar] [CrossRef]
- Sena, L.A.; Caraballo, M.M.; Rossi, A.M.; Soares, G.A. Synthesis and characterization of biocomposites with different hydroxyapatite-collagen ratios. J. Mater. Sci. Mater. Med. 2009, 20, 2395–2400. [Google Scholar] [CrossRef] [PubMed]
- Wei, J.; Li, Y. Tissue engineering scaffold material of nano-apatite crystals and polyamide composite. Eur. Polym. J. 2004, 40, 509–515. [Google Scholar]
- Ciapetti, G.; Ambrosio, L.; Savarino, L.; Granchi, D.; Cenni, E.; Baldini, N.; Pagani, S.; Guizzardi, S.; Causa, F.; Giunti, A. Osteoblast growth and function in porous poly epsilon -caprolactone matrices for bone repair: A preliminary study. Biomaterials 2003, 24, 3815–3824. [Google Scholar] [CrossRef]
- Zhang, R.; Ma, P.X. Poly(alpha-hydroxyl acids)/hydroxyapatite porous composites for bone-tissue engineering. I. Preparation and morphology. J. Biomed. Mater. Res. 1999, 44, 446–455. [Google Scholar] [CrossRef]
- De Santis, R.; Russo, A.; Gloria, A.; D’Amora, U.; Russo, T.; Panseri, S.; Sandri, M.; Tampieri, A.; Marcacci, M.; Dediu, V.A.; et al. Towards the Design of 3D Fiber-Deposited Poly(-caprolactone)/Iron-Doped Hydroxyapatite Nanocomposite Magnetic Scaffolds for Bone Regeneration. J. Biomed. Nanotechnol. 2015, 11, 1236–1246. [Google Scholar] [CrossRef] [PubMed]
- Shi, S.F.; Jia, J.F.; Guo, X.K.; Zhao, Y.P.; Chen, D.S.; Guo, Y.Y.; Cheng, T.; Zhang, X.L. Biocompatibility of chitosan-coated iron oxide nanoparticles with osteoblast cells. Int. J. Nanomed. 2012, 7, 5593–5602. [Google Scholar]
- Hung, H.S.; Chu, M.Y.; Lin, C.H.; Wu, C.C.; Hsu, S.H. Mediation of the migration of endothelial cells and fibroblasts on polyurethane nanocomposites by the activation of integrin-focal adhesion kinase signaling. J. Biomed. Mater. Res. A 2012, 100, 26–37. [Google Scholar] [CrossRef]
- Morouço, P.; Biscaia, S.; Viana, T.; Franco, M.; Malça, C.; Mateus, A.; Moura, C.; Ferreira, F.C.; Mitchell, G.; Alves, N.M. Fabrication of Poly (-caprolactone) Scaffolds Reinforced with Cellulose Nanofibers, with and without the Addition of Hydroxyapatite Nanoparticles. BioMed Res. Int. 2016, 2016, 10. [Google Scholar] [CrossRef] [Green Version]
- Szcześ, A.; Hołysz, L.; Chibowski, E. Synthesis of hydroxyapatite for biomedical applications. Adv. Colloid Interface Sci. 2017, 249, 321–330. [Google Scholar] [CrossRef]
- Demirtaş, T.T.; Irmak, G.; Gümüşderelioğlu, M. A bioprintable form of chitosan hydrogel for bone tissue engineering. Biofabrication 2017, 9, 035003. [Google Scholar] [CrossRef]
- Chaudhuri, O.; Gu, L.; Klumpers, D.; Darnell, M.; Bencherif, S.A.; Weaver, J.C.; Huebsch, N.; Lee, H.P.; Lippens, E.; Duda, G.N.; et al. Hydrogels with tunable stress relaxation regulate stem cell fate and activity. Nat. Mater. 2016, 15, 326–334. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Katarivas Levy, G.; Ong, J.; Birch, M.A.; Justin, A.W.; Markaki, A.E. Albumin-Enriched Fibrin Hydrogel Embedded in Active Ferromagnetic Networks Improves Osteoblast Differentiation and Vascular Self-Organisation. Polymers 2019, 11, 1743. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Russo, T.; D’Amora, U.; Gloria, A.; Tunesi, M.; Sandri, M.; Rodilossi, S.; Albani, D.; Forloni, G.; Giordano, C.; Cigada, A.; et al. Systematic Analysis of Injectable Materials and 3D Rapid Prototyped Magnetic Scaffolds: From CNS Applications to Soft and Hard Tissue Repair/Regeneration. Procedia Eng. 2013, 59, 233–239. [Google Scholar] [CrossRef] [Green Version]
- Gloria, A.; Russo, T.; D’Amora, U.; Santin, M.; De Santis, R.; Ambrosio, L. Customised multiphasic nucleus/annulus scaffold for intervertebral disc repair/regeneration. Connect. Tissue Res. 2020, 61, 152–162. [Google Scholar] [CrossRef]
- Fu, S.; Ni, P.; Wang, B.; Chu, B.; Zheng, L.; Luo, F.; Luo, J.; Qian, Z. Injectable and thermo-sensitive PEG-PCL-PEG copolymer/collagen/n-HA hydrogel composite for guided bone regeneration. Biomaterials 2012, 33, 4801–4809. [Google Scholar] [CrossRef]
- Kinneberg, K.R.; Nelson, A.; Stender, M.E.; Aziz, A.H.; Mozdzen, L.C.; Harley, B.A.; Bryant, S.J.; Ferguson, V.L. Reinforcement of Mono- and Bi-layer Poly(Ethylene Glycol) Hydrogels with a Fibrous Collagen Scaffold. Ann. Biomed. Eng. 2015, 43, 2618–2629. [Google Scholar] [CrossRef] [Green Version]
- Qu, Y.; Wang, B.; Chu, B.; Liu, C.; Rong, X.; Chen, H.; Peng, J.; Qian, Z. Injectable and Thermosensitive Hydrogel and PDLLA Electrospun Nanofiber Membrane Composites for Guided Spinal Fusion. ACS Appl. Mater. Interfaces 2018, 10, 4462–4470. [Google Scholar] [CrossRef]
- Gruber, R.M.; Krohn, S.; Mauth, C.; Dard, M.; Molenberg, A.; Lange, K.; Perske, C.; Schliephake, H. Mandibular reconstruction using a calcium phosphate/polyethylene glycol hydrogel carrier with BMP-2. J. Clin. Periodontol. 2014, 41, 820–826. [Google Scholar] [CrossRef]
- Yadid, M.; Feiner, R.; Dvir, T. Gold Nanoparticle-Integrated Scaffolds for Tissue Engineering and Regenerative Medicine. Nano Lett. 2019, 19, 2198–2206. [Google Scholar] [CrossRef]
- Hu, M.; Chen, J.; Li, Z.Y.; Au, L.; Hartland, G.V.; Li, X.; Marquez, M.; Xia, Y. Gold nanostructures: Engineering their plasmonic properties for biomedical applications. Chem Soc. Rev. 2006, 35, 1084–1094. [Google Scholar] [CrossRef]
- Vial, S.; Reis, R.L.; Oliveira, J.M. Recent advances using gold nanoparticles as a promising multimodal tool for tissue engineering and regenerative medicine. Curr. Opin. Solid State Mater. Sci. 2017, 21, 92–112. [Google Scholar] [CrossRef] [Green Version]
- Hung, H.S.; Wu, C.C.; Chien, S.; Hsu, S.H. The behavior of endothelial cells on polyurethane nanocomposites and the associated signaling pathways. Biomaterials 2009, 30, 1502–1511. [Google Scholar] [CrossRef]
- Hung, H.S.; Tang, C.M.; Lin, C.H.; Lin, S.Z.; Chu, M.Y.; Sun, W.S.; Kao, W.C.; Hsien-Hsu, H.; Huang, C.Y.; Hsu, S.H. Biocompatibility and favorable response of mesenchymal stem cells on fibronectin-gold nanocomposites. PLoS ONE 2013, 8, e65738. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hung, H.S.; Chang, C.H.; Chang, C.J.; Tang, C.M.; Kao, W.C.; Lin, S.Z.; Hsieh, H.H.; Chu, M.Y.; Sun, W.S.; Hsu, S.H. In vitro study of a novel nanogold-collagen composite to enhance the mesenchymal stem cell behavior for vascular regeneration. PLoS ONE 2014, 9, e104019. [Google Scholar] [CrossRef]
- Khosravi, A.; Ghasemi-Mobarakeh, L.; Mollahosseini, H.; Ajalloueian, F.; Masoudi Rad, M.; Norouzi, M.-R.; Sami Jokandan, M.; Khoddami, A.; Chronakis, I.S. Immobilization of silk fibroin on the surface of PCL nanofibrous scaffolds for tissue engineering applications. J. Appl. Polym. Sci. 2018, 135, 46684. [Google Scholar] [CrossRef] [Green Version]
- Lee, D.; Heo, D.N.; Lee, S.J.; Heo, M.; Kim, J.; Choi, S.; Park, H.-K.; Park, Y.G.; Lim, H.-N.; Kwon, I.K. Poly(lactide-co-glycolide) nanofibrous scaffolds chemically coated with gold-nanoparticles as osteoinductive agents for osteogenesis. Appl. Surf. Sci. 2018, 432, 300–307. [Google Scholar] [CrossRef]
- Yi, C.; Liu, D.; Fong, C.C.; Zhang, J.; Yang, M. Gold nanoparticles promote osteogenic differentiation of mesenchymal stem cells through p38 MAPK pathway. ACS Nano 2010, 4, 6439–6448. [Google Scholar] [CrossRef]
- Zhou, J.; Zhang, Y.; Li, L.; Fu, H.; Yang, W.; Yan, F. Human β-defensin 3-combined gold nanoparticles for enhancement of osteogenic differentiation of human periodontal ligament cells in inflammatory microenvironments. Int. J. Nanomed. 2018, 13, 555–567. [Google Scholar] [CrossRef] [Green Version]
- Ross, R.D.; Roeder, R.K. Binding affinity of surface functionalized gold nanoparticles to hydroxyapatite. J. Biomed. Mater. Res. A 2011, 99, 58–66. [Google Scholar] [CrossRef]
- Lee, S.J.; Lee, H.J.; Kim, S.Y.; Seok, J.M.; Lee, J.H.; Kim, W.D.; Kwon, I.K.; Park, S.Y.; Park, S.A. In situ gold nanoparticle growth on polydopamine-coated 3D-printed scaffolds improves osteogenic differentiation for bone tissue engineering applications: In vitro and in vivo studies. Nanoscale 2018, 10, 15447–15453. [Google Scholar] [CrossRef] [Green Version]
- Borciani, G.; Montalbano, G.; Baldini, N.; Cerqueni, G.; Vitale-Brovarone, C.; Ciapetti, G. Co–culture systems of osteoblasts and osteoclasts: Simulating in vitro bone remodeling in regenerative approaches. Acta Biomater. 2020, 108, 22–45. [Google Scholar] [CrossRef] [PubMed]
- Safari, B.; Aghanejad, A.; Roshangar, L.; Davaran, S. Osteogenic effects of the bioactive small molecules and minerals in the scaffold-based bone tissue engineering. Colloids Surf. B Biointerfaces 2020, 198, 111462. [Google Scholar] [CrossRef] [PubMed]
- Editorial Office, I. International Journal of Molecular Science 2018 Best Paper Award. Int. J. Mol. Sci. 2018, 19, 3694. [Google Scholar]
- Sugiura, F.; Kitoh, H.; Ishiguro, N. Osteogenic potential of rat mesenchymal stem cells after several passages. Biochem. Biophys. Res. Commun. 2004, 316, 233–239. [Google Scholar] [CrossRef] [PubMed]
- Ishikawa, H.; Kitoh, H.; Sugiura, F.; Ishiguro, N. The effect of recombinant human bone morphogenetic protein-2 on the osteogenic potential of rat mesenchymal stem cells after several passages. Acta Orthop. 2007, 78, 285–292. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Frassica, M.T.; Jones, S.K.; Diaz-Rodriguez, P.; Hahn, M.S.; Grunlan, M.A. Incorporation of a silicon-based polymer to PEG-DA templated hydrogel scaffolds for bioactivity and osteoinductivity. Acta Biomater. 2019, 99, 100–109. [Google Scholar] [CrossRef]
- Kutikov, A.B.; Skelly, J.D.; Ayers, D.C.; Song, J. Templated repair of long bone defects in rats with bioactive spiral-wrapped electrospun amphiphilic polymer/hydroxyapatite scaffolds. ACS Appl. Mater. Interfaces 2015, 7, 4890–4901. [Google Scholar] [CrossRef]
- Gao, G.; Schilling, A.F.; Yonezawa, T.; Wang, J.; Dai, G.; Cui, X. Bioactive nanoparticles stimulate bone tissue formation in bioprinted three-dimensional scaffold and human mesenchymal stem cells. Biotechnol. J. 2014, 9, 1304–1311. [Google Scholar] [CrossRef]
- Hsieh, S.C.; Chen, H.J.; Hsu, S.H.; Yang, Y.C.; Tang, C.M.; Chu, M.Y.; Lin, P.Y.; Fu, R.H.; Kung, M.L.; Chen, Y.W.; et al. Prominent Vascularization Capacity of Mesenchymal Stem Cells in Collagen-Gold Nanocomposites. ACS Appl. Mater. Interfaces 2016, 8, 28982–29000. [Google Scholar] [CrossRef]
- Hsu, S.H.; Tang, C.M.; Tseng, H.J. Biocompatibility of poly (ether) urethane-gold nanocomposites. J. Biomed. Mater. Res. Part A 2006, 79, 759–770. [Google Scholar] [CrossRef]
- Ding, D.C.; Shyu, W.C.; Chiang, M.F.; Lin, S.Z.; Chang, Y.C.; Wang, H.J.; Su, C.Y.; Li, H. Enhancement of neuroplasticity through upregulation of beta1-integrin in human umbilical cord-derived stromal cell implanted stroke model. Neurobiol. Dis. 2007, 27, 339–353. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, S.; Ahmed, N.; Rungatscher, A.; Linardi, D.; Kulsoom, B.; Innamorati, G.; Meo, S.A.; Gebrie, M.A.; Mani, R.; Merigo, F.; et al. Cocoa Flavonoids Reduce Inflammation and Oxidative Stress in a Myocardial Ischemia-Reperfusion Experimental Model. Antioxidants 2020, 9, 167. [Google Scholar] [CrossRef] [Green Version]
- Namba, T.; Koike, H.; Murakami, K.; Aoki, M.; Makino, H.; Hashiya, N.; Ogihara, T.; Kaneda, Y.; Kohno, M.; Morishita, R. Angiogenesis induced by endothelial nitric oxide synthase gene through vascular endothelial growth factor expression in a rat hindlimb ischemia model. Circulation 2003, 108, 2250–2257. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zikherman, J.; Doan, K.; Parameswaran, R.; Raschke, W.; Weiss, A. Quantitative differences in CD45 expression unmask functions for CD45 in B-cell development, tolerance, and survival. Proc. Natl. Acad. Sci. USA 2012, 109, E3–E12. [Google Scholar] [CrossRef] [Green Version]
- Hung, H.S.; Yang, Y.C.; Lin, Y.C.; Lin, S.Z.; Kao, W.C.; Hsieh, H.H.; Chu, M.Y.; Fu, R.H.; Hsu, S.H. Regulation of human endothelial progenitor cell maturation by polyurethane nanocomposites. Biomaterials 2014, 35, 6810–6821. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.W.; Hsieh, S.C.; Yang, Y.C.; Hsu, S.H.; Kung, M.L.; Lin, P.Y.; Hsieh, H.H.; Lin, C.H.; Tang, C.M.; Hung, H.S. Functional engineered mesenchymal stem cells with fibronectin-gold composite coated catheters for vascular tissue regeneration. Nanomedicine 2018, 14, 699–711. [Google Scholar] [CrossRef] [PubMed]
- Zhu, W.; Chu, C.; Kuddannaya, S.; Yuan, Y.; Walczak, P.; Singh, A.; Song, X.; Bulte, J.W.M. In Vivo Imaging of Composite Hydrogel Scaffold Degradation Using CEST MRI and Two-Color NIR Imaging. Adv. Funct. Mater. 2019, 29, 1903753. [Google Scholar] [CrossRef]
- Ding, J.; Zhang, J.; Li, J.; Li, D.; Xiao, C.; Xiao, H.; Yang, H.; Zhuang, X.; Chen, X. Electrospun polymer biomaterials. Prog. Polym. Sci. 2019, 90, 1–34. [Google Scholar] [CrossRef]
- Oteri, G.; Pizzino, G.; Pisano, M.; Peditto, M.; Squadrito, F.; Bitto, A. Polyethylene glycol formulations show different soft tissue remodeling and angiogenesis features. Tissue Eng. Part. A 2015, 21, 580–585. [Google Scholar] [CrossRef] [Green Version]
- Cai, L.; Wang, Q.; Gu, C.; Wu, J.; Wang, J.; Kang, N.; Hu, J.; Xie, F.; Yan, L.; Liu, X.; et al. Vascular and micro-environmental influences on MSCS-coral hydroxyapatite construct-based bone tissue engineering. Biomaterials 2011, 32, 8497–8505. [Google Scholar] [CrossRef]
- Xia, Y.; Sun, J.; Zhao, L.; Zhang, F.; Liang, X.J.; Guo, Y.; Weir, M.D.; Reynolds, M.A.; Gu, N.; Xu, H.H.K. Magnetic field and nano-scaffolds with stem cells to enhance bone regeneration. Biomaterials 2018, 183, 151–170. [Google Scholar] [CrossRef]
- Ito, T.; Sasaki, M.; Taguchi, T. Enhanced ALP activity of MG63 cells cultured on hydroxyapatite-poly(ethylene glycol) hydrogel composites prepared using EDTA-OH. Biomed. Mater. 2015, 10, 015025. [Google Scholar] [CrossRef]
- Mahmoud, N.S.; Ahmed, H.H.; Mohamed, M.R.; Amr, K.S.; Aglan, H.A.; Ali, M.A.M.; Tantawy, M.A. Role of nanoparticles in osteogenic differentiation of bone marrow mesenchymal stem cells. Cytotechnology 2020, 72, 1–22. [Google Scholar] [CrossRef] [PubMed]
- Liang, H.; Xu, X.; Feng, X.; Ma, L.; Deng, X.; Wu, S.; Liu, X.; Yang, C. Gold nanoparticles-loaded hydroxyapatite composites guide osteogenic differentiation of human mesenchymal stem cells through Wnt/β-catenin signaling pathway. Int. J. Nanomed. 2019, 14, 6151–6163. [Google Scholar] [CrossRef] [Green Version]
- Tetè, S.; Zara, S.; Vinci, R.; Zizzari, V.; Di Tore, U.; Mastrangelo, F.; Cataldi, A.; Gherlone, E. Vascular endothelial growth factor and e-nitric oxide synthase-mediated regenerative response occurring upon autologous and heterologous bone grafts. Int. J. Immunopathol. Pharm. 2009, 22, 1105–1116. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Wang, Y.; Wang, Z.; Qi, Y.; Li, L.; Zhang, P.; Chen, X.; Huang, Y. Composite PLA/PEG/nHA/Dexamethasone Scaffold Prepared by 3D Printing for Bone Regeneration. Macromol. Biosci. 2018, 18, e1800068. [Google Scholar] [CrossRef] [PubMed]
- Malpuech-Brugère, C.; Nowacki, W.; Daveau, M.; Gueux, E.; Linard, C.; Rock, E.; Lebreton, J.; Mazur, A.; Rayssiguier, Y. Inflammatory response following acute magnesium deficiency in the rat. Biochim. Biophys. Acta 2000, 1501, 91–98. [Google Scholar] [CrossRef] [Green Version]
- Mak, I.T.; Dickens, B.F.; Komarov, A.M.; Wagner, T.L.; Phillips, T.M.; Weglicki, W.B. Activation of the neutrophil and loss of plasma glutathione during Mg-deficiency-modulation by nitric oxide synthase inhibition. Mol. Cell Biochem. 1997, 176, 35–39. [Google Scholar] [CrossRef]
- Yu, L.; Rowe, D.W.; Perera, I.P.; Zhang, J.; Suib, S.L.; Xin, X.; Wei, M. Intrafibrillar Mineralized Collagen-Hydroxyapatite-Based Scaffolds for Bone Regeneration. ACS Appl. Mater. Interfaces 2020, 12, 18235–18249. [Google Scholar] [CrossRef]
- Heo, D.N.; Ko, W.K.; Lee, H.R.; Lee, S.J.; Lee, D.; Um, S.H.; Lee, J.H.; Woo, Y.H.; Zhang, L.G.; Lee, D.W.; et al. Titanium dental implants surface-immobilized with gold nanoparticles as osteoinductive agents for rapid osseointegration. J. Colloid Interface Sci. 2016, 469, 129–137. [Google Scholar] [CrossRef]
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Shen, C.-C.; Hsu, S.-h.; Chang, K.-B.; Yeh, C.-A.; Chang, H.-C.; Tang, C.-M.; Yang, Y.-C.; Hsieh, H.-H.; Hung, H.-S. Physical Gold Nanoparticle-Decorated Polyethylene Glycol-Hydroxyapatite Composites Guide Osteogenesis and Angiogenesis of Mesenchymal Stem Cells. Biomedicines 2021, 9, 1632. https://doi.org/10.3390/biomedicines9111632
Shen C-C, Hsu S-h, Chang K-B, Yeh C-A, Chang H-C, Tang C-M, Yang Y-C, Hsieh H-H, Hung H-S. Physical Gold Nanoparticle-Decorated Polyethylene Glycol-Hydroxyapatite Composites Guide Osteogenesis and Angiogenesis of Mesenchymal Stem Cells. Biomedicines. 2021; 9(11):1632. https://doi.org/10.3390/biomedicines9111632
Chicago/Turabian StyleShen, Chiung-Chyi, Shan-hui Hsu, Kai-Bo Chang, Chun-An Yeh, Hsiang-Chun Chang, Cheng-Ming Tang, Yi-Chin Yang, Hsien-Hsu Hsieh, and Huey-Shan Hung. 2021. "Physical Gold Nanoparticle-Decorated Polyethylene Glycol-Hydroxyapatite Composites Guide Osteogenesis and Angiogenesis of Mesenchymal Stem Cells" Biomedicines 9, no. 11: 1632. https://doi.org/10.3390/biomedicines9111632