Enhancing X-ray Attenuation of 3D Printed Gelatin Methacrylate (GelMA) Hydrogels Utilizing Gold Nanoparticles for Bone Tissue Engineering Applications
Abstract
:1. Introduction
2. Materials and Methods
2.1. Preparation of Gelatin Methacrylate (GelMA), GelMA, and GelMA-AuNPs Pre-polymer Solution
2.2. Evaluation of in vitro Cytocompatibility, Mechanical Properties, and µCT Visibility of GelMA and GelMA-AuNP Bulk Hydrogels
2.3. 3D Printing of GelMA and GelMA-AuNP Scaffolds
2.4. In vitro Evaluation of Osteogenic Differentiation of MSCs on GelMA and GelMA-AuNPs
2.5. In Vitro Imaging of the GelMA and GelMA-AuNP Scaffolds in µCT
2.6. Statistical Method
3. Results
3.1. Characterization of GelMA-AuNPs Bulk Hydrogel
3.2. 3D Printing of GelMA and GelMA-AuNP Scaffolds
3.3. In Vitro Evaluation of Osteogenic Differentiation of MSCs on GelMA and GelMA-AuNPs
3.4. In Vitro Imaging of the 3D Printed GelMA and GelMA-AuNP Scaffolds in µCT
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Chen, B.-Q.; Kankala, R.K.; Chen, A.-Z.; Yang, D.-Z.; Cheng, X.-X.; Jiang, N.-N.; Zhu, K.; Wang, S.-B. Investigation of silk fibroin nanoparticle-decorated poly (l-lactic acid) composite scaffolds for osteoblast growth and differentiation. Int. J. Nanomed. 2017, 12, 1877. [Google Scholar] [CrossRef]
- Kankala, R.; Lu, F.-J.; Liu, C.-G.; Zhang, S.-S.; Chen, A.-Z.; Wang, S.-B. Effect of icariin on engineered 3d-printed porous scaffolds for cartilage repair. Materials. 2018, 11, 1390. [Google Scholar] [CrossRef]
- Nam, S.Y.; Ricles, L.M.; Suggs, L.J.; Emelianov, S.Y. Imaging Strategies for Tissue Engineering Applications. Tissue Eng. Part B Rev. 2015, 21, 88–103. [Google Scholar] [CrossRef]
- Janke, H.P.; Güvener, N.; Dou, W.; Tiemessen, D.M.; YantiSetiasti, A.; Cremers, J.G.O.; Borm, P.J.A.; Feitz, W.F.J.; Heerschap, A.; Kiessling, F. Labeling of Collagen Type I Templates with a Naturally Derived Contrast Agent for Noninvasive MR Imaging in Soft Tissue Engineering. Adv. Healthc. Mater. 2018, 7, 1800605. [Google Scholar] [CrossRef]
- Mastrogiacomo, S.; Güvener, N.; Dou, W.; Alghamdi, H.S.; Camargo, W.A.; Cremers, J.G.O.; Borm, P.J.A.; Heerschap, A.; Oosterwijk, E.; Jansen, J.A. A theranostic dental pulp capping agent with improved MRI and CT contrast and biological properties. Acta Biomater. 2017, 62, 340–351. [Google Scholar] [CrossRef]
- Mastrogiacomo, S.; Dou, W.; Koshkina, O.; Boerman, O.C.; Jansen, J.A.; Heerschap, A.; Srinivas, M.; Walboomers, X.F. Perfluorocarbon/Gold Loading for Noninvasive in Vivo Assessment of Bone Fillers Using (19)F Magnetic Resonance Imaging and Computed Tomography. ACS Appl. Mater. Interfaces 2017. [Google Scholar] [CrossRef]
- Kankala, R.K.; Zhu, K.; Sun, X.-N.; Liu, C.-G.; Wang, S.-B.; Chen, A.-Z. Cardiac tissue engineering on the nanoscale. ACS Biomater. Sci. Eng. 2018, 4, 800–818. [Google Scholar] [CrossRef]
- Carlos, J.; Vega, D. La; Häfeli, U.O. Utilization of nanoparticles as X-ray contrast agents for diagnostic imaging applications. Contrast Media Mol. Imaging. 2015. [Google Scholar] [CrossRef]
- Rumiński, S.; Ostrowska, B.; Jaroszewicz, J.; Skirecki, T.; Włodarski, K.; Święszkowski, W.; Lewandowska-Szumieł, M. Three-dimensional printed polycaprolactone-based scaffolds provide an advantageous environment for osteogenic differentiation of human adipose-derived stem cells. J. Tissue Eng. Regen. Med. 2018, 12, e473–e485. [Google Scholar] [CrossRef]
- Cuijpers, V.M.J.I.; Alghamdi, H.S.; Van Dijk, N.W.M.; Jaroszewicz, J.; Walboomers, X.F.; Jansen, J.A. Osteogenesis around CaP-coated titanium implants visualized using 3D histology and micro-computed tomography. J. Biomed. Mater. Res. Part A 2015, 103, 3463–3473. [Google Scholar] [CrossRef]
- Costantini, M.; Testa, S.; Mozetic, P.; Barbetta, A.; Fuoco, C.; Fornetti, E.; Tamiro, F.; Bernardini, S.; Jaroszewicz, J.; Swieszkowski, W.; et al. Microfluidic-enhanced 3D bioprinting of aligned myoblast-laden hydrogels leads to functionally organized myofibers in vitro and in vivo. Biomaterials 2017, 131, 98–110. [Google Scholar] [CrossRef]
- Jones, A.C.; Arns, C.H.; Sheppard, A.P.; Hutmacher, D.W.; Milthorpe, B.K.; Knackstedt, M.A. Assessment of bone ingrowth into porous biomaterials using MICRO-CT. Biomaterials 2007, 28, 2491–2504. [Google Scholar] [CrossRef]
- Ho, S.T.; Hutmacher, D.W. A comparison of micro CT with other techniques used in the characterization of scaffolds. Biomaterials 2006, 27, 1362–1376. [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]
- Heo, D.N.; Ko, W.-K.; Bae, M.S.; Lee, J.B.; Lee, D.-W.; Byun, W.; Lee, C.H.; Kim, E.-C.; Jung, B.-Y.; Kwon, I.K. Enhanced bone regeneration with a gold nanoparticle–hydrogel complex. J. Mater. Chem. B 2014, 2, 1584. [Google Scholar] [CrossRef]
- Schuurman, W.; Levett, P.A.; Pot, M.W.; van Weeren, P.R.; Dhert, W.J.A.; Hutmacher, D.W.; Melchels, F.P.W.; Klein, T.J.; Malda, J. Gelatin-methacrylamide hydrogels as potential biomaterials for fabrication of tissue-engineered cartilage constructs. Macromol. Biosci. 2013, 13, 551–561. [Google Scholar] [CrossRef]
- Levett, P.A.; Melchels, F.P.W.; Schrobback, K.; Hutmacher, D.W.; Malda, J.; Klein, T.J. A biomimetic extracellular matrix for cartilage tissue engineering centered on photocurable gelatin, hyaluronic acid and chondroitin sulfate. Acta Biomater. 2014, 10, 214–223. [Google Scholar] [CrossRef] [Green Version]
- Rinoldi, C.; Costantini, M.; Kijeńska-Gawrońska, E.; Testa, S.; Fornetti, E.; Heljak, M.; Ćwiklińska, M.; Buda, R.; Baldi, J.; Cannata, S. Tendon Tissue Engineering: Effects of Mechanical and Biochemical Stimulation on Stem Cell Alignment on Cell-Laden Hydrogel Yarns. Adv. Healthc. Mater. 2019, 1801218. [Google Scholar] [CrossRef]
- Kang, H.; Shih, Y.R.V.; Hwang, Y.; Wen, C.; Rao, V.; Seo, T.; Varghese, S. Mineralized gelatin methacrylate-based matrices induce osteogenic differentiation of human induced pluripotent stem cells. Acta Biomater. 2014, 10, 4961–4970. [Google Scholar] [CrossRef] [Green Version]
- Celikkin, N.; Mastrogiacomo, S.; Jaroszewicz, J.; Walboomers, X.F.; Swieszkowski, W. Gelatin methacrylate scaffold for bone tissue engineering: The influence of polymer concentration. J. Biomed. Mater. Res. Part A 2017. [Google Scholar] [CrossRef]
- Visser, J.; Gawlitta, D.; Benders, K.E.M.; Toma, S.M.H.; Pouran, B.; van Weeren, P.R.; Dhert, W.J.A.; Malda, J. Endochondral bone formation in gelatin methacrylamide hydrogel with embedded cartilage-derived matrix particles. Biomaterials 2015, 37, 174–182. [Google Scholar] [CrossRef]
- Yue, K.; Santiago, G.T.; Tamayol, A.; Annabi, N.; Khademhosseini, A.; Hospital, W.; Arabia, S.; Trujillo-De Santiago, G.; Alvarez, M.M.; Tamayol, A.; et al. Synthesis, properties, and biomedical applications of gelatin methacryloyl (GelMA) hydrogels. Biomaterials 2015, 73, 254–271. [Google Scholar] [CrossRef] [Green Version]
- Wang, H.; Zhou, L.; Liao, J.; Tan, Y.; Ouyang, K.; Ning, C.; Ni, G.; Tan, G. Cell-laden photocrosslinked GelMA-DexMA copolymer hydrogels with tunable mechanical properties for tissue engineering. J. Mater. Sci. Mater. Med. 2014, 25, 2173–2183. [Google Scholar] [CrossRef]
- Murphy, C.M.; Haugh, M.G. The effect of mean pore size on cell attachment, proliferation and migration in collagen glycosaminoglycan scaffolds for tissue engineering. Biomaterials 2010, 31, 461–466. [Google Scholar] [CrossRef]
- Kankala, R.K.; Zhu, K.; Li, J.; Wang, C.-S.; Wang, S.-B.; Chen, A.-Z. Fabrication of arbitrary 3D components in cardiac surgery: From macro-, micro-to nanoscale. Biofabrication 2017, 9, 32002. [Google Scholar] [CrossRef]
- Kankala, R.; Xu, X.-M.; Liu, C.-G.; Chen, A.-Z.; Wang, S.-B. 3D-printing of microfibrous porous scaffolds based on hybrid approaches for bone tissue engineering. Polymers. 2018, 10, 807. [Google Scholar] [CrossRef]
- Ji, S.; Guvendiren, M. Recent Advances in Bioink Design for 3D Bioprinting of Tissues and Organs. Front. Bioeng. Biotechnol. 2017, 5, 23. [Google Scholar] [CrossRef]
- Negrini, N.C.; Bonnetier, M.; Giatsidis, G.; Orgill, D.P.; Farè, S.; Marelli, B. Tissue-mimicking gelatin scaffolds by alginate sacrificial templates for adipose tissue engineering. Acta Biomater. 2019. [Google Scholar]
- Loessner, D.; Meinert, C.; Kaemmerer, E.; Martine, L.C.; Yue, K.; Levett, P. a; Klein, T.J.; Melchels, F.P.W.; Khademhosseini, A.; Hutmacher, D.W. Functionalization, preparation and use of cell-laden gelatin methacryloyl-based hydrogels as modular tissue culture platforms. Nat. Protoc. 2016, 11, 727–746. [Google Scholar] [CrossRef]
- Nichol, J.W.; Koshy, S.T.; Bae, H.; Hwang, C.M.; Yamanlar, S.; Khademhosseini, A. Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials 2010, 31, 5536–5544. [Google Scholar] [CrossRef] [Green Version]
- Moreau, D.; Villain, A.; Bachy, M.; Proudhon, H.; Ku, D.N.; Hannouche, D.; Petite, H.; Corté, L. In vivo evaluation of the bone integration of coated poly(vinyl-alcohol) hydrogel fiber implants. J. Mater. Sci. Mater. Med. 2017, 28. [Google Scholar] [CrossRef]
- He, B.; Ou, Y.; Chen, S.; Zhao, W.; Zhou, A.; Zhao, J.; Li, H.; Jiang, D.; Zhu, Y. Designer bFGF-incorporated D-form self-assembly peptide nanofiber scaffolds to promote bone repair. Mater. Sci. Eng. C 2017, 74, 451–458. [Google Scholar] [CrossRef]
- Lohmann, P.; Willuweit, A.; Neffe, A.T.; Geisler, S.; Gebauer, T.P.; Beer, S.; Coenen, H.H.; Fischer, H.; Hermanns-Sachweh, B.; Lendlein, A.; et al. Bone regeneration induced by a 3D architectured hydrogel in a rat critical-size calvarial defect. Biomaterials 2017, 113, 158–169. [Google Scholar] [CrossRef]
- Bair, R.J.; Bair, E.; Viswanathan, A.N. A radiopaque polymer hydrogel used as a fiducial marker in gynecologic-cancer patients receiving brachytherapy. Brachytherapy 2015, 14, 876–880. [Google Scholar] [CrossRef] [Green Version]
- Fatimi, A.; Zehtabi, F.; Lerouge, S. Optimization and characterization of injectable chitosan-iodixanol- based hydrogels for the embolization of blood vessels. Soc. Biomater. 2015, 1–12. [Google Scholar] [CrossRef]
- Boelen, E.J.H.; Koole, L.H.; van Rhijn, L.; van Hooy-Corstjens, C.S.J. Towards a Functional Radiopaque Hydrogel for Nucleus Pulposus Replacement. J. Biomed. Mater. Res. Part B Appl. Biomater. 2007, 83, 440–450. [Google Scholar] [CrossRef]
- Hertig, G.; Zehnder, M.; Woloszyk, A.; Mitsiadis, T.A.; Ivica, A.; Weber, F.E. Iodixanol as a contrast agent in a fibrin hydrogel for endodontic applications. Front. Physiol. 2017, 8, 1–6. [Google Scholar] [CrossRef]
- Pan, Y.; Neuss, S.; Leifert, A.; Fischler, M.; Wen, F.; Simon, U.; Schmid, G.; Brandau, W.; Jahnen-Dechent, W. Size-dependent cytotoxicity of gold nanoparticles. Small 2007, 3, 1941–1949. [Google Scholar] [CrossRef]
- Mironava, T.; Hadjiargyrou, M.; Simon, M.; Jurukovski, V.; Rafailovich, M.H. Gold nanoparticles cellular toxicity and recovery: Effect of size, concentration and exposure time. Nanotoxicology 2010, 4, 120–137. [Google Scholar] [CrossRef]
- Pernodet, N.; Fang, X.; Sun, Y.; Bakhtina, A.; Ramakrishnan, A.; Sokolov, J.; Ulman, A.; Rafailovich, M. Adverse effects of citrate/gold nanoparticles on human dermal fibroblasts. Small 2006, 2, 766–773. [Google Scholar] [CrossRef]
- Chang, M.; Shiau, A.; Chen, Y.; Chang, C.; Chen, H.H.; Wu, C. Increased apoptotic potential and dose-enhancing effect of gold nanoparticles in combination with single-dose clinical electron beams on tumor-bearing mice. Cancer Sci. 2008, 99, 1479–1484. [Google Scholar] [CrossRef] [Green Version]
- Soenen, S.J.; Rivera-Gil, P.; Montenegro, J.-M.; Parak, W.J.; De Smedt, S.C.; Braeckmans, K. Cellular toxicity of inorganic nanoparticles: Common aspects and guidelines for improved nanotoxicity evaluation. Nano Today 2011, 6, 446–465. [Google Scholar] [CrossRef]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Celikkin, N.; Mastrogiacomo, S.; Walboomers, X.F.; Swieszkowski, W. Enhancing X-ray Attenuation of 3D Printed Gelatin Methacrylate (GelMA) Hydrogels Utilizing Gold Nanoparticles for Bone Tissue Engineering Applications. Polymers 2019, 11, 367. https://doi.org/10.3390/polym11020367
Celikkin N, Mastrogiacomo S, Walboomers XF, Swieszkowski W. Enhancing X-ray Attenuation of 3D Printed Gelatin Methacrylate (GelMA) Hydrogels Utilizing Gold Nanoparticles for Bone Tissue Engineering Applications. Polymers. 2019; 11(2):367. https://doi.org/10.3390/polym11020367
Chicago/Turabian StyleCelikkin, Nehar, Simone Mastrogiacomo, X. Frank Walboomers, and Wojciech Swieszkowski. 2019. "Enhancing X-ray Attenuation of 3D Printed Gelatin Methacrylate (GelMA) Hydrogels Utilizing Gold Nanoparticles for Bone Tissue Engineering Applications" Polymers 11, no. 2: 367. https://doi.org/10.3390/polym11020367