Microstructured and Degradable Bacterial Cellulose–Gelatin Composite Membranes: Mineralization Aspects and Biomedical Relevance
Abstract
:1. Introduction
- A BC membrane can be efficiently merged with porous GEL through a simple procedure we propose, using a water-based system free of including additional chemicals;
- Short incubation in supersaturated simulated body fluid (SBF) promotes the formation of calcium phosphate (CaP)-based minerals on and within BC–GEL composites; and
- Human embryo fibroblast cells attaches differently on differently structured GELs.
2. Materials and Methods
2.1. Reagents and Materials
2.2. BC–GEL Membranes
2.3. In Situ Mineralization
2.4. Fourier Transform Infrared (FTIR) Spectroscopy
2.5. X-Ray Diffraction (XRD) Spectroscopy
2.6. Scanning Electron Microscopy (SEM) and Energy Dispersive X-Ray (EDX) Spectroscopy
2.7. Confocal Fluorescence Microscopy (CFM)
2.8. Swelling and Degradation Test
2.9. Cell Testing
2.9.1. Cell Line
2.9.2. Preparation of Eluates and Cellular Exposure
2.9.3. Direct Exposure of Cells with Samples
2.9.4. Bioreduction into Formazan
2.9.5. Analysis in Direct Contact
2.9.6. Statistical Analysis
3. Results and Discussion
3.1. BC Modification: Oxidation and Conjugation with GEL
3.2. Microstructural Assessment
3.3. Mineralization
3.4. Physiological Data
3.5. Cell Testing
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Ul-Islam, M.; Khan, S.; Ullah, M.W.; Park, J.K. Bacterial cellulose composites: Synthetic strategies and multiple applications in bio-medical and electro-conductive fields. Biotechnol. J. 2015, 10, 1847–1861. [Google Scholar] [CrossRef] [PubMed]
- Neacsu, P.; Staras, A.; Voicu, S.; Ionascu, I.; Soare, T.; Uzun, S.; Cojocaru, V.; Pandele, A.; Croitoru, S.; Miculescu, F.; et al. Characterization and In Vitro and In Vivo Assessment of a Novel Cellulose Acetate-Coated Mg-Based Alloy for Orthopedic Applications. Materials 2017, 10, 686. [Google Scholar] [CrossRef] [PubMed]
- Pandele, A.M.; Comanici, F.E.; Carp, C.A.; Miculescu, F.; Voicu, S.I.; Thakur, V.K.; Serban, B.C. Synthesis and characterization of cellulose acetate-hydroxyapatite micro and nano composites membranes for water purification and biomedical applications. Vacuum 2017, 146, 599–605. [Google Scholar] [CrossRef]
- Pandele, A.M.; Neacsu, P.; Cimpean, A.; Staras, A.I.; Miculescu, F.; Iordache, A.; Voicu, S.I.; Thakur, V.K.; Toader, O.D. Cellulose acetate membranes functionalized with resveratrol by covalent immobilization for improved osseointegration. Appl. Surf. Sci. 2018, 438, 2–13. [Google Scholar] [CrossRef]
- Wu, J.; Zheng, Y.; Wen, X.; Lin, Q.; Chen, X.; Wu, Z. Silver nanoparticle/bacterial cellulose gel membranes for antibacterial wound dressing: Investigation in vitro and in vivo. Biomed. Mater. 2014, 9, 035005. [Google Scholar] [CrossRef] [PubMed]
- Tronser, T.; Laromaine, A.; Roig, A.; Levkin, P.A. Bacterial Cellulose Promotes Long-Term Stemness of mESC. ACS Appl. Mater. Interfaces 2018, 10, 16260–16269. [Google Scholar] [CrossRef] [PubMed]
- Yang, J.; Du, M.; Wang, L.; Li, S.; Wang, G.; Yang, X.; Zhang, L.; Fang, Y.; Zheng, W.; Yang, G.; et al. Bacterial Cellulose as a Supersoft Neural Interfacing Substrate. ACS Appl. Mater. Interfaces 2018, 10, 33049–33059. [Google Scholar] [CrossRef]
- Lin, W.-C.; Lien, C.-C.; Yeh, H.-J.; Yu, C.-M.; Hsu, S. Bacterial cellulose and bacterial cellulose–chitosan membranes for wound dressing applications. Carbohydr. Polym. 2013, 94, 603–611. [Google Scholar] [CrossRef]
- Millon, L.E.; Wan, W.K. The polyvinyl alcohol–bacterial cellulose system as a new nanocomposite for biomedical applications. J. Biomed. Mater. Res. Part B Appl. Biomater. 2006, 79, 245–253. [Google Scholar] [CrossRef]
- Véliz, D.S.; Alam, C.; Toivola, D.M.; Toivakka, M.; Alam, P. On the non-linear attachment characteristics of blood to bacterial cellulose/kaolin biomaterials. Colloids Surf. B Biointerfaces 2014, 116, 176–182. [Google Scholar] [CrossRef]
- Andrade, F.K.; Silva, J.P.; Carvalho, M.; Castanheira, E.M.S.; Soares, R.; Gama, M. Studies on the hemocompatibility of bacterial cellulose. J. Biomed. Mater. Res. Part A 2011, 98, 554–566. [Google Scholar] [CrossRef] [PubMed]
- Orelma, H.; Morales, L.O.; Johansson, L.S.; Hoeger, I.C.; Filpponen, I.; Castro, C.; Rojas, O.J.; Laine, J. Affibody conjugation onto bacterial cellulose tubes and bioseparation of human serum albumin. RSC Adv. 2014, 4, 51440–51450. [Google Scholar] [CrossRef]
- Cai, Z.; Kim, J. Preparation and Characterization of Novel Bacterial Cellulose/Gelatin Scaffold for Tissue Regeneration Using Bacterial Cellulose Hydrogel. J. Nanotechnol. Eng. Med. 2010, 1, 021002. [Google Scholar] [CrossRef]
- Barud, H.O.; Barud, H.D.; Cavicchioli, M.; do Amaral, T.S.; de Oliveira Junior, O.B.; Santos, D.M.; Petersen, A.L.; Celes, F.; Borges, V.M.; de Oliveira, C.I.; et al. Preparation and characterization of a bacterial cellulose/silk fibroin sponge scaffold for tissue regeneration. Carbohydr. Polym. 2015, 128, 41–51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, J.; Zhao, L.; Zhang, A.; Huang, Y.; Tavakoli, J.; Tang, Y. Novel Bacterial Cellulose/Gelatin Hydrogels as 3D Scaffolds for Tumor Cell Culture. Polymers 2018, 10, 581. [Google Scholar] [CrossRef]
- Jing, W.; Chunxi, Y.; Yizao, W.; Honglin, L.; Fang, H.; Kerong, D.; Yuan, H. Laser Patterning of Bacterial Cellulose Hydrogel and its Modification With Gelatin and Hydroxyapatite for Bone Tissue Engineering. Soft Mater. 2013, 11, 173–180. [Google Scholar] [CrossRef]
- Khan, S.; Ul-Islam, M.; Ikram, M.; Ullah, M.W.; Israr, M.; Subhan, F.; Kim, Y.; Jang, J.H.; Yoon, S.; Park, J.K. Three-dimensionally microporous and highly biocompatible bacterial cellulose–gelatin composite scaffolds for tissue engineering applications. RSC Adv. 2016, 6, 110840–110849. [Google Scholar] [CrossRef]
- Gorgieva, S.; Kokol, V. Processing of gelatin-based cryogels with improved thermomechanical resistance, pore size gradient, and high potential for sustainable protein drug release. J. Biomed. Mater. Res. A 2015, 103, 1119–1130. [Google Scholar] [CrossRef]
- Gorgieva, S.; Vuherer, T.; Kokol, V. Autofluorescence-aided assessment of integration and μ-structuring in chitosan/gelatin bilayer membranes with rapidly mineralized interface in relevance to guided tissue regeneration. Mater. Sci. Eng. C 2018, 93, 226–241. [Google Scholar] [CrossRef]
- Qiao, H.; Guo, T.; Zheng, Y.; Zhao, L.; Sun, Y.; Liu, Y.; Xie, Y. A novel microporous oxidized bacterial cellulose/arginine composite and its effect on behavior of fibroblast/endothelial cell. Carbohydr. Polym. 2018, 184, 323–332. [Google Scholar] [CrossRef]
- Wu, J.; Zheng, Y.; Yang, Z.; Lin, Q.; Qiao, K.; Chen, X.; Peng, Y. Influence of dialdehyde bacterial cellulose with the nonlinear elasticity and topology structure of ECM on cell adhesion and proliferation. RSC Adv. 2014, 4, 3998–4009. [Google Scholar] [CrossRef]
- Shao, W.; Wu, J.; Liu, H.; Ye, S.; Jiang, L.; Liu, X. Novel bioactive surface functionalization of bacterial cellulose membrane. Carbohydr. Polym. 2017, 178, 270–276. [Google Scholar] [CrossRef] [PubMed]
- Wen, X.; Zheng, Y.; Wu, J.; Wang, L.N.; Yuan, Z.; Peng, J.; Meng, H. Immobilization of collagen peptide on dialdehyde bacterial cellulose nanofibers via covalent bonds for tissue engineering and regeneration. Int. J. Nanomed. 2015, 10, 4623–4637. [Google Scholar]
- Fan, Q.G.; Lewis, D.M.; Tapley, K.N. Characterization of Cellulose Aldehyde Using Fourier Transform Infrared Spectroscopy. J. Appl. Polym. Sci. 2001, 82, 1195–1202. [Google Scholar] [CrossRef]
- Dawlee, S.; Sugandhi, A.; Balakrishnan, B.; Labarre, D.; Jayakrishnan, A. Oxidized Chondroitin Sulfate-Cross-Linked Gelatin Matrixes: A New Class of Hydrogels. Biomacromolecules 2005, 6, 2040–2048. [Google Scholar] [CrossRef] [PubMed]
- Wu, Y.; Yuan, L.; Sheng, N.A.; Gu, Z.Q.; Feng, W.H.; Yin, H.Y.; Morsi, Y.; Mo, X.M. A soft tissue adhesive based on aldehyde-sodium alginate and amino-carboxymethyl chitosan preparation through the Schiff reaction. Front. Mater. Sci. 2017, 11, 215–222. [Google Scholar] [CrossRef]
- Gorgieva, S.; Štrancar, J.; Kokol, V. Evaluation of surface/interface-related physicochemical and microstructural properties of gelatin 3D scaffolds, and their influence on fibroblast growth and morphology. J. Biomed. Mater. Res. Part A 2014, 102, 3986–3997. [Google Scholar] [CrossRef]
- Miller, L.M.; Bourassa, M.W.; Smith, R.J. FTIR spectroscopic imaging of protein aggregation in living cells. Biochim. Biophys. Acta Biomembr. 2013, 1828, 2339–2346. [Google Scholar] [CrossRef] [Green Version]
- Payne, K.J.; Veis, A. Fourier transform ir spectroscopy of collagen and gelatin solutions: Deconvolution of the amide I band for conformational studies. Biopolymers 1988, 27, 1749–1760. [Google Scholar] [CrossRef]
- Sakai, A.; Murayama, Y.; Fujiwara, K.; Fujisawa, T.; Sasaki, S.; Kidoaki, S.; Yanagisawa, M. Increasing Elasticity through Changes in the Secondary Structure of Gelatin by Gelation in a Microsized Lipid Space. ACS Central Sci. 2018, 4, 477–483. [Google Scholar] [CrossRef]
- Milner-White, E.J. The Partial Charge of the Nitrogen Atom in Peptide Bond; Cambridge University Press: Cambridge, UK, 1997. [Google Scholar]
- Treesuppharat, W.; Rojanapanthu, P.; Siangsanoh, C.; Manuspiya, H.; Ummartyotin, S. Synthesis and characterization of bacterial cellulose and gelatin-based hydrogel composites for drug-delivery systems. Biotechnol. Rep. 2017, 15, 84–91. [Google Scholar] [CrossRef] [PubMed]
- Gorgieva, S.; Modic, M.; Dovgan, B.; Kaisersberger-Vincek, M.; Kokol, V. Plasma-Activated Polypropylene Mesh-Gelatin Scaffold Composite as Potential Implant for Bioactive Hernia Treatment. Plasma Process. Polym. 2015, 12, 237–251. [Google Scholar] [CrossRef]
- Koshy, S.T.; Ferrante, T.C.; Lewin, S.A.; Mooney, D.J. Injectable, porous, and cell-responsive gelatin cryogels. Biomaterials 2014, 35, 2477–2487. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Clasen, A.B.S.; Ruyter, I.E. Quantitative Determination of Type A and Type B Carbonate in Human Deciduous and Permanent Enamel by Means of Fourier Transform Infrared Spectrometry. Adv. Dent. Res. 1997, 11, 523–527. [Google Scholar] [CrossRef] [PubMed]
- Boanini, E.; Gazzano, M.; Bigi, A. Ionic substitutions in calcium phosphates synthesized at low temperature. Acta Biomater. 2010, 6, 1882–1894. [Google Scholar] [CrossRef]
- Djomehri, S.I.; Candell, S.; Case, T.; Browning, A.; Marshall, G.W.; Yun, W.; Lau, S.H.; Webb, S.; Ho, S.P. Mineral Density Volume Gradients in Normal and Diseased Human Tissues. PLoS ONE 2015, 10, e0121611. [Google Scholar] [CrossRef]
- Berzina-Cimdina, L.; Borodajenko, N. Research of Calcium Phosphates Using Fourier Transform Infrared Spectroscopy. In Infrared Spectroscopy—Materials Science, Engineering and Technology; IntechOpen: London, UK, 2012. [Google Scholar]
- Alobeedallah, H.; Ellis, J.L.; Rohanizadeh, R.; Coster, H.; Dehghani, F. Preparation of Nanostructured Hydroxyapatite in Organic Solvents for Clinical Applications. Trends Biomater. Artif. Organs 2011, 25, 12–19. [Google Scholar]
- Hutchens, S.A.; Benson, R.S.; Evans, B.R.; O’Neill, H.M.; Rawn, C.J. Biomimetic synthesis of calcium-deficient hydroxyapatite in a natural hydrogel. Biomaterials 2006, 27, 4661–4670. [Google Scholar] [CrossRef]
- Arellano-Jiménez, M.J.; García-García, R.; Reyes-Gasga, J. Synthesis and hydrolysis of octacalcium phosphate and its characterization by electron microscopy and X-ray diffraction. J. Phys. Chem. Solids 2009, 70, 390–395. [Google Scholar] [CrossRef]
- Lin, X.; de Groot, K.; Wang, D.; Hu, Q.; Wismeijer, D.; Liu, Y. A Review Paper on Biomimetic Calcium Phosphate Coatings. Eng. Life Sci. 2017, 17, 1108–1117. [Google Scholar] [CrossRef]
- Song, J.E.; Su, J.; Loureiro, A.; Martins, M.; Cavaco-Paulo, A.; Kim, H.R.; Silva, C. Ultrasound-assisted swelling of bacterial cellulose. Eng. Life Sci. 2017, 17, 1108–1117. [Google Scholar] [CrossRef]
- Qiao, K.; Zheng, Y.; Guo, S.; Tan, J.; Chen, X.; Li, J.; Xu, D.; Wang, J. Hydrophilic nanofiber of bacterial cellulose guided the changes in the micro-structure and mechanical properties of nf-BC/PVA composites hydrogels. Compos. Sci. Technol. 2015, 118, 47–54. [Google Scholar] [CrossRef]
- Ma, S.; Adayi, A.; Liu, Z.; Li, M.; Wu, M.; Xiao, L.; Sun, Y.; Cai, Q.; Yang, X.; Zhang, X.; et al. Asymmetric Collagen/chitosan Membrane Containing Minocycline-loaded Chitosan Nanoparticles for Guided Bone Regeneration. Sci. Rep. 2016, 6, 31822. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qasim, S.B.; Delaine-Smith, R.M.; Fey, T.; Rawlinson, A.; Rehman, I.U. Freeze gelated porous membranes for periodontal tissue regeneration. Acta Biomater. 2015, 23, 317–328. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Charles, K.; Honibald, E.N.; Reddy, N.R.; Palani, A.; Ramamurthy, R.D.; Sankaralingam, T. Role of matrix metalloproteinases (MMPS) in periodontitis and its management. J. Indian Acad. Dent. Spec. Res. 2014, 2, 65. [Google Scholar]
- Bacakova, L.; Filova, E.; Parizek, M.; Ruml, T.; Svorcik, V. Modulation of cell adhesion, proliferation and differentiation on materials designed for body implants. Biotechnol. Adv. 2011, 29, 739–767. [Google Scholar] [CrossRef] [PubMed]
- Davidenko, N.; Schuster, C.F.; Bax, D.V.; Farndale, R.W.; Hamaia, S.; Best, S.M.; Cameron, R.E. Evaluation of cell binding to collagen and gelatin: A study of the effect of 2D and 3D architecture and surface chemistry. J. Mater. Sci. Mater. Med. 2016, 27, 148. [Google Scholar] [CrossRef] [PubMed]
- Babo, P.S.; Ab, R.L.R.; Gomes, M.E. Periodontal tissue engineering: Current strategies and the role of platelet rich hemoderivatives. J. Mater. Chem. B 2017, 5, 3617. [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
Gorgieva, S.; Hribernik, S. Microstructured and Degradable Bacterial Cellulose–Gelatin Composite Membranes: Mineralization Aspects and Biomedical Relevance. Nanomaterials 2019, 9, 303. https://doi.org/10.3390/nano9020303
Gorgieva S, Hribernik S. Microstructured and Degradable Bacterial Cellulose–Gelatin Composite Membranes: Mineralization Aspects and Biomedical Relevance. Nanomaterials. 2019; 9(2):303. https://doi.org/10.3390/nano9020303
Chicago/Turabian StyleGorgieva, Selestina, and Silvo Hribernik. 2019. "Microstructured and Degradable Bacterial Cellulose–Gelatin Composite Membranes: Mineralization Aspects and Biomedical Relevance" Nanomaterials 9, no. 2: 303. https://doi.org/10.3390/nano9020303