Self-assembly of multiscale anisotropic hydrogels through interfacial polyionic complexation.
alginate
automated collector
cerium oxide nanoparticles
chitosan
fibrous hydrogels
gellan gum
interfacial polyionic complexation
kappa carrageenan
polysaccharides
Journal
Journal of biomedical materials research. Part A
ISSN: 1552-4965
Titre abrégé: J Biomed Mater Res A
Pays: United States
ID NLM: 101234237
Informations de publication
Date de publication:
12 2020
12 2020
Historique:
received:
07
01
2020
revised:
06
04
2020
accepted:
19
04
2020
pubmed:
18
5
2020
medline:
9
11
2021
entrez:
18
5
2020
Statut:
ppublish
Résumé
Polysaccharides are explored for various tissue engineering applications due to their inherent cytocompatibility and ability to form bulk hydrogels. However, bulk hydrogels offer poor control over their microarchitecture and multiscale hierarchy, parameters important to recreate extracellular matrix-mimetic microenvironment. Here, we developed a versatile platform technology to self-assemble oppositely charged polysaccharides into multiscale fibrous hydrogels with controlled anisotropic microarchitecture. We employed polyionic complexation through microfluidic flow of positively charged polysaccharide, chitosan, along with one of the three negatively charged polysaccharides: alginate, gellan gum, and kappa carrageenan. These hydrogels were composed of microscale fibers, which in turn were made of submicron fibrils confirming multiscale hierarchy. Fibrous hydrogels showed strong tensile mechanical properties, which were further modulated by encapsulation of shape-specific antioxidant cerium oxide nanoparticles (CNPs). Specifically, hydrogels with chitosan and gellan gum showed more than eight times higher tensile strength compared to the other two pairs. Incorporation of sphere-shaped cerium oxide nanoparticles in chitosan and gellan gum further reinforced fibrous hydrogels and increased their tensile strength by 40%. Altogether, our automated hydrogel fabrication platform allows fabrication of bioinspired biomaterials with scope for one-step encapsulation of small molecules and nanoparticles without chemical modification or use of chemical crosslinkers.
Substances chimiques
Biocompatible Materials
0
Hydrogels
0
Carrageenan
9000-07-1
Chitosan
9012-76-4
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2504-2518Subventions
Organisme : NCI NIH HHS
ID : P30CA047904
Pays : United States
Informations de copyright
© 2020 Wiley Periodicals, Inc.
Références
Abbah, S. A., Liu, J., Lam, R. W. M., Goh, J. C. H., & Wong, H. K. (2012). In vivo bioactivity of rhBMP-2 delivered with novel polyelectrolyte complexation shells assembled on an alginate microbead core template. Journal of Controlled Release, 162(2), 364-372.
Amaike, M., Senoo, Y., & Yamamoto, H. (1998). Sphere, honeycomb, regularly spaced droplet and fiber structures of polyion complexes of chitosan and gellan. Macromolecular Rapid Communications, 19(6), 287-289.
Annabi, N., Shin, S. R., Tamayol, A., Miscuglio, M., Bakooshli, M. A., Assmann, A., … Khademhosseini, A. (2016). Highly elastic and conductive human-based protein hybrid hydrogels. Advanced Materials, 28(1), 40-49.
Arenales-Sierra, I. M., Lobato-Calleros, C., Vernon-Carter, E. J., Hernandez-Rodriguez, L., & Alvarez-Ramirez, J. (2019). Calcium alginate beads loaded with Mg(OH)(2) improve L. casei viability under simulated gastric condition. Lwt-Food Science and Technology, 112.
Bidarra, S. J., Barrias, C. C., & Granja, P. L. (2014). Injectable alginate hydrogels for cell delivery in tissue engineering. Acta Biomaterialia, 10, 1646-1662.
Bryant, S. J., Nuttelman, C. R., & Anseth, K. S. (2000). Cytocompatibility of UV and visible light photoinitiating systems on cultured NIH/3T3 fibroblasts in vitro. Journal of Biomaterials Science-Polymer Edition, 11(5), 439-457.
Costa-Almeida, R., Gasperini, L., Borges, J., Babo, P. S., Rodrigues, M. T., Mano, J. F., … Gomes, M. E. (2017). Microengineered multicomponent hydrogel fibers: Combining polyelectrolyte complexation and microfluidics. ACS Biomaterials Science & Engineering, 3(7), 1322-1331.
Coutinho, D. F., Sant, S., Shakiba, M., Wang, B., Gomes, M. E., Neves, N. M., … Khademhosseini, A. (2012). Microfabricated photocrosslinkable polyelectrolyte-complex of chitosan and methacrylated gellan gum. Journal of Materials Chemistry, 22(33), 17262-17271.
Cutiongco, M. F., Choo, R. K., Shen, N. J., Chua, B. M., Sju, E., Choo, A. W., … Yim, E. K. (2015). Composite scaffold of poly(vinyl alcohol) and interfacial polyelectrolyte complexation fibers for controlled biomolecule delivery. Frontiers in Bioengineering and Biotechnology, 3, 3.
Cutiongco, M. F., Teo, B. K., & Yim, E. K. (2015). Composite scaffolds of interfacial polyelectrolyte fibers for temporally controlled release of biomolecules. Journal of Visualized Experiments, 102, e53079.
Duarte, A. R. C., Correlo, V. M., Oliveira, J. M., & Reis, R. L. (2016). Recent developments on chitosan applications in regenerative medicine. Biomaterials from nature for advanced devices and therapies (pp. 221-243). Hoboken, NJ: John Wiley & Sons Inc.
Jin, S. C., Li, K., Xia, C. L., & Li, J. Z. (2019). Sodium alginate-assisted route to antimicrobial biopolymer film combined with aminoclay for enhanced mechanical behaviors. Industrial Crops and Products, 135, 271-282.
Leong, M. F., Toh, J. K., Du, C., Narayanan, K., Lu, H. F., Lim, T. C., … Ying, J. Y. (2013). Patterned prevascularised tissue constructs by assembly of polyelectrolyte hydrogel fibres. Nature Communications, 4, 2353.
Lin, Z., Wu, J., Qiao, W., Zhao, Y., Wong, K. H. M., Chu, P. K., … Yeung, K. W. K. (2018). Precisely controlled delivery of magnesium ions thru sponge-like monodisperse PLGA/nano-MgO-alginate core-shell microsphere device to enable in-situ bone regeneration. Biomaterials, 174, 1-16.
McNamara, M. C., Sharifi, F., Wrede, A. H., Kimlinger, D. F., Thomas, D. G., Vander Wiel, J. B., … Hashemi, N. N. (2017). Microfibers as physiologically relevant platforms for creation of 3D cell cultures. Macromolecular Bioscience, 17, 12.
Meier, C., & Welland, M. E. (2011). Wet-spinning of amyloid protein nanofibers into multifunctional high-performance biofibers. Biomacromolecules, 12(10), 3453-3359.
Mendes, A. C., Strohmenger, T., Goycoolea, F., & Chronakis, I. S. (2017). Electrostatic self-assembly of polysaccharides into nanofibers. Colloids and Surfaces a-Physicochemical and Engineering Aspects, 531, 182-188.
Narayanan, K., Leck, K. J., Gao, S. J., & Wan, A. C. A. (2009). Three-dimensional reconstituted extracellular matrix scaffolds for tissue engineering. Biomaterials, 30(26), 4309-4317.
Onoe, H., & Takeuchi, S. (2015). Cell-laden microfibers for bottom-up tissue engineering. Drug Discovery Today, 20(2), 236-246.
Patel, A., Xue, Y. F., Hartley, R., Sant, V., Eles, J. R., Cui, X. T., … Sant, S. (2018). Hierarchically aligned fibrous hydrogel films through microfluidic self-assembly of graphene and polysaccharides. Biotechnology and Bioengineering, 115(10), 2654-2667.
Pinheiro, A. C., Bourbon, A. I., Medeiros, B. G. D., da Silva, L. H. M., da Silva, M. C. H., Carneiro-da-Cunha, M. G., … Vicente, A. A. (2012). Interactions between kappa-carrageenan and chitosan in nanolayered coatings-Structural and transport properties. Carbohydrate Polymers, 87(2), 1081-1090.
Puspoki, Z., Storath, M., Sage, D., & Unser, M. (2016). Transforms and operators for directional bioimage analysis: A survey. Advances in Anatomy, Embryology, and Cell Biology, 219, 69-93.
Rabanel, J. M., Bertrand, N., Sant, S., Louati, S., & Hildgen, P. (2006). Polysaccharide hydrogels for the preparation of immunoisolated cell delivery systems. Polysaccharides for Drug Delivery and Pharmaceutical Applications, 934, 305-339.
Razdan, S., Patra, P. K., Kar, S., Ci, L., Vajtai, R., Kukovecz, A., … Ajayan, P. M. (2009). Ionically self-assembled polyelectrolyte-based carbon nanotube fibers. Chemistry of Materials, 21(14), 3062-3071.
Sant, S., Coutinho, D. F., Gaharwar, A. K., Neves, N. M., Reis, R. L., Gomes, M. E., & Khademhosseini, A. (2017). Self-assembled hydrogel fiber bundles from oppositely charged polyelectrolytes mimic micro-/nanoscale hierarchy of collagen. Advanced Functional Materials, 27, 1606273.
Silva, J. M., Caridade, S. G., Oliveira, N. M., & Reis, R. L. (2015). Chitosan-Alginate multilayered films with gradients of physicochemical cues. Journal of Materials Chemistry B, 3, 4555.
Stevens, L. R., Gilmore, K. J., Wallace, G. G., & In Het Panhuis, M. (2016). Tissue engineering with gellan gum. Biomaterials Science, 4(9), 1276-1290.
Verma, D., Katti, K. S., & Katti, D. R. (2009). Polyelectrolyte-complex nanostructured fibrous scaffolds for tissue engineering. Materials Science and Engineering: C, 29(7), 2079-2084.
Voron'ko, N. G., Derkach, S. R., Vovk, M. A., & Tolstoy, P. M. (2016). Formation of kappa-carrageenan-gelatin polyelectrolyte complexes studied by H-1 NMR, UV spectroscopy and kinematic viscosity measurements. Carbohydrate Polymers, 151, 1152-1161.
Wan, A. C., Leong, M. F., Toh, J. K., Zheng, Y., & Ying, J. Y. (2012). Multicomponent fibers by multi-interfacial polyelectrolyte complexation. Advanced Healthcare Materials, 1(1), 101-105.
Wan, A. C. A., Cutiongco, M. F. A., Tai, B. C. U., Leong, M. F., Lu, H. F., & Yim, E. K. F. (2016). Fibers by interfacial polyelectrolyte complexation-Processes, materials and applications. Materials Today, 19(8), 437-450.
Wan, A. C. A., Liao, I. C., Yim, E. K. F., & Leong, K. W. (2004). Mechanism of fiber formation by interfacial polyelectrolyte complexation. Macromolecules, 37(18), 7019-7025.
Wan, A. C. A., Yim, E. K. F., Liao, I. C., Le Visage, C., & Leong, K. W. (2004). Encapsulation of biologics in self-assembled fibers as biostructural units for tissue engineering. Journal of Biomedical Materials Research Part A, 71A(4), 586-595.
Xue, Y., Balmuri, S. R., Patel, A., Sant, V., & Sant, S. (2018). Synthesis, physico-chemical characterization, and antioxidant effect of PEGylated cerium oxide nanoparticles. Drug Delivery and Translational Research, 8(2), 357-367.
Xue, Y., St Hilaire, C., Hortells, L., Phillippi, J. A., Sant, V., & Sant, S. (2017). Shape-specific nanoceria mitigate oxidative stress-induced calcification in primary human valvular interstitial cell culture. Cellular and Molecular Bioengineering, 10(5), 483-500.
Yamada, M., Sugaya, S., Naganuma, Y., & Seki, M. (2012). Microfluidic synthesis of chemically and physically anisotropic hydrogel microfibers for guided cell growth and networking. Soft Matter, 8(11), 3122-3130.
Yamamoto, H., Horita, C., Senoo, Y., Nishida, A., & Ohkawa, K. (2001). Polyion complex fiber and capsule formed by self-assembly of poly-l-lysine and gellan at solution interfaces. Journal of Applied Polymer Science, 79(3), 437-446.
Yamamoto, H., Ohkawa, K., Nakamura, E., Miyamoto, K., & Komai, T. (2003). Preparation of polyion complex capsule and fiber of chitosan and gellan-sulfate at aqueous interface. Bulletin of the Chemical Society of Japan, 76(10), 2053-2057.
Yamamoto, H., & Senoo, Y. (2000). Polyion complex fiber and capsule formed by self-assembly of chitosan and gellan at solution interfaces. Macromolecular Chemistry and Physics, 201(1), 84-92.
Yamanlar, S., Sant, S., Boudou, T., Picart, C., & Khademhosseini, A. (2011). Surface functionalization of hyaluronic acid hydrogels by polyelectrolyte multilayer films. Biomaterials, 32(24), 5590-5599.
Yim, E. K., Wan, A. C., Le Visage, C., Liao, I. C., & Leong, K. W. (2006). Proliferation and differentiation of human mesenchymal stem cell encapsulated in polyelectrolyte complexation fibrous scaffold. Biomaterials, 27(36), 6111-6622.
Zhang, Y. S., & Khademhosseini, A. (2017). Advances in engineering hydrogels. Science, 356, 6337.
Zhu, F. B., Cheng, L. B., Yin, J., Wu, Z. L., Qian, J., Fu, J. Z., & Zheng, Q. (2016). 3D printing of ultratough polyion complex hydrogels. ACS Applied Materials & Interfaces, 8(45), 31304-31310.
Zou, J., & Kim, F. (2012). Self-assembly of two-dimensional nanosheets induced by interfacial polyionic complexation. ACS Nano, 6(12), 10606-10613.