Abstract
Objective
The insufficient stability of alginate-chitosan (ALG-CS) microcapsules in biorelevant media limits their applications in the biomedical field. Attempts were made to improve the membrane stability of ALG-CS microcapsules by noncovalent crosslinking with tannic acid.
Results
The membrane stability of ALG-CS microcapsules in culture medium and serum was significantly improved by crosslinking with tannic acid. Moreover, the reason for the significant improvement in membrane stability had been demonstrated to be that the stability of chitosan-tannic acid (CS-TA) polyelectrolyte complexes was less affected by the competitive binding of those weak acid ions such as HCO3−. In addition, the optimal conditions for preparing alginate-chitosan-tannic acid (ALG-CS-TA) microcapsules were tannic acid concentration of 0.5% (w/v) and pH = 7.
Conclusion
The study provides a novel approach for improving the stability of the ALG-CS microcapsules in biorelevant media to expand their scope of application in the biological field.
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References
Abulateefeh SR, Taha MO (2015) Enhanced drug encapsulation and extended release profiles of calcium-alginate nanoparticles by using tannic acid as a bridging cross-linking agent. J Microencapsul 32(1):96–105. https://doi.org/10.3109/02652048.2014.985343
Arora S, Budhiraja RD (2012) Chitosan-alginate microcapsules of amoxicillin for gastric stability and mucoadhesion. Adv Pharm Technol Res 3(1):68–74. https://doi.org/10.4103/2231-4040.93555
Bai ZX, Wang TY, Zheng X, Huang YP, Chen YN, Dan WH (2021) High strength and bioactivity polyvinyl alcohol/collagen composite hydrogel with tannic acid as cross-linker. Polym Eng Sci 61(1):278–287. https://doi.org/10.1002/pen.25574
Chen L, Zhang Y, Li S, Wang XL et al (2014) Effect of plasma components on the stability and permeability of microcapsule. J Biomed Mater Res A 102(7):2408–2416. https://doi.org/10.1002/jbm.a.34907
Chui CY, Odeleye A, Nguyen L, Kasoju N, Soliman E, Ye H (2019) Electrosprayed genipin cross-linked alginate-chitosan microcarriers for ex vivo expansion of mesenchymal stem cells. J Biomed Mater Res A 107(1):122–133. https://doi.org/10.1002/jbm.a.36539
Eleftheriadou D, Evans RE, Atkinson E, Abdalla A, Gavins FKH, Boyd AS, Williams GR, Knowles JC, Roberton VH, Phillips JB (2022) An alginate-based encapsulation system for delivery of therapeutic cells to the CNS. RSC Adv 12(7):4005–4015. https://doi.org/10.1039/d1ra08563h
Gierszewska M, Ostrowska-Czubenko J, Chrzanowska E (2018) Ph-responsive chitosan/alginate polyelectrolyte complex membranes reinforced by tripolyphosphate. Eur Polym J 101:282–290. https://doi.org/10.1016/j.eurpolymj.2018.02.031
Gur SD, Idil N, Aksoz N (2018) Optimization of enzyme co-immobilization with sodium alginate and glutaraldehyde-activated chitosan beads. Appl Biochem Biotechnol 184(2):538–552. https://doi.org/10.1007/s12010-017-2566-5
Karakas CY, Ordu HR, Bozkurt F, Karadag A (2022) Electrosprayed chitosan-coated alginate-pectin beads as potential system for colon-targeted delivery of ellagic acid. J Sci Food Agric 102(3):965–975. https://doi.org/10.1002/jsfa.11430
Kim MJ, Park HS, Kim JW, Lee EY, Rhee M, You YH, Khang G, Park CG, Yoon KH (2021) Suppression of fibrotic reactions of chitosan-alginate microcapsules containing porcine islets by dexamethasone surface coating. Endocrinol Metab 36(1):146–156. https://doi.org/10.3803/EnM.2021.879
Lam PL, Gambari R (2014) Advanced progress of microencapsulation technologies: in vivo and in vitro models for studying oral and transdermal drug deliveries. J Control Release 178:25–45. https://doi.org/10.1016/j.jconrel.2013.12.028
Lertsutthiwong P, Rojsitthisak P (2011) Chitosan-alginate nanocapsules for encapsulation of turmeric oil. Pharmazie 66(12):911–915. https://doi.org/10.1691/ph.2011.1068
Li L, Zhang Y, Pan X (2017) Preparation and characterization of Alginate-Chitosan microcapsule for hepatocyte culture. Methods Mol Biol 1479:199–206. https://doi.org/10.1007/978-1-4939-6364-5_15
Li Z, Chen L, Xu MT, Ma Y, Chen L, Dai FY (2020) Double crosslinking hydrogel with tunable properties for potential biomedical application. J Polym Res 27(9):262. https://doi.org/10.1007/s10965-020-02242-x
Liu BX, Wang Y, Yang F, Wang X, Shen H, Cui HX, Wu DC (2016a) Construction of a controlled-release delivery system for pesticides using biodegradable PLA-based microcapsules. Colloids Surf B Biointerfaces 144:38–45. https://doi.org/10.1016/j.colsurfb.2016.03.084
Liu WL, Liu W, Ye AQ, Peng SF, Wei FQ, Liu CM, Han JZ (2016b) Environmental stress stability of microencapsules based on liposomes decorated with chitosan and sodium alginate. Food Chem 196:396–404. https://doi.org/10.1016/j.foodchem.2015.09.050
Lou RY, Yu WT, Song YZ, Ren Y, Zheng HZ, Guo X, Lin YF, Pan GY, Wang XL, Ma XJ (2017) Fabrication of stable galactosylated alginate microcapsules via covalent coupling onto hydroxyl groups for hepatocytes applications. Carbohydr Polym 155:456–465. https://doi.org/10.1016/j.carbpol.2016.08.098
Lu J, Zhu DH, Li LJ (2022) Evaluation of hydromechanical and functional properties of diversion-type microcapsule-suspension bioreactor for bioartificial liver. Int J Artif Organs 45(3):309–321. https://doi.org/10.1177/03913988211066502
Lv GJ, Sun ZJ, Li SY, Yu WT, **e YB, Zhang Y, **e HG, Li XX, Wang W, Ma XJ (2009) Permeability changes of the cell-contained microcapsules visualized by confocal laser scanning microscope. J Biomed Mater Res A 90(3):773–783. https://doi.org/10.1002/jbm.a.32115
Ma Y, Zhang Y, Zhao S, Wang Y et al (2012) Modeling and optimization of membrane preparation conditions of the alginate-based microcapsules with response surface methodology. J Biomed Mater Res A 100A(4):989–998. https://doi.org/10.1002/jbm.a.34032
Mahou R, Passemard S, Carvello M, Petrelli A, Noverraz F, Gerber-Lemaire S, Wandrey C (2016) Contribution of polymeric materials to progress in xenotransplantation of microencapsulated cells: a review. Xenotransplantation 23(3):179–201. https://doi.org/10.1111/xen.12240
Martau GA, Mihai M, Vodnar DC (2019) The use of chitosan, alginate, and pectin in the biomedical and food sector-biocompatibility, bioadhesiveness, and biodegradability. Polymers 11(11):1837. https://doi.org/10.3390/polym11111837
Meng QY, Zhong SL, Wang J, Gao Y, Cui XJ (2023) Advances in chitosan-based microcapsules and their applications. Carbohydr Polym 300:120265. https://doi.org/10.1016/j.carbpol.2022.120265
Murakami D, Kobayashi M, Higaki Y, **nai H, Takahara A (2016) Swollen structure and electrostatic interactions of polyelectrolyte brush in aqueous solution. Polymer 98:464–469. https://doi.org/10.1016/j.polymer.2016.04.041
Park JW, Park KH, Seo S (2019) Natural polyelectrolyte complex-based Ph-dependent delivery carriers using alginate and chitosan. J Appl Polym Sci 136(43):48143. https://doi.org/10.1002/app.48143
Ren Y, **e HG, Liu XC, Yang F, Yu WT, Ma XJ (2016) Tuning the formation and stability of microcapsules by environmental conditions and chitosan structure. Int J Biol Macromol 91:1090–1100. https://doi.org/10.1016/j.ijbiomac.2016.06.034
Shutava TG, Lvov YM (2006) Nano-engineered microcapsules of tannic acid and chitosan for protein encapsulation. J Nanosci Nanotechnol 6(6):1655–1661. https://doi.org/10.1166/jnn.2006.225
Sionkowska A, Kaczmarek B, Lewandowska K (2014) Modification of collagen and chitosan mixtures by the addition of tannic acid. J Mol Liq 199:318–323. https://doi.org/10.1016/j.molliq.2014.09.028
Trinh CK, Schnabel W (1993) Ionic strength dependence of the stability of polyelectrolyte complexes: its importance for the isolation of multiply charged polymers. Angew Makromol Chem 212(1):167–179. https://doi.org/10.1002/apmc.1993.052120115
Wang YH, Hu R, Guo YL, Qin WH, Zhang XM, Hua L, Yang Y (2021) Preparation, evaluation, and in vitro release of chitosan-alginate tanshinone self-microemulsifying sustained-release microcapsules. Technol Health Care 29(4):687–695. https://doi.org/10.3233/THC-202529
**e XL, Zhou XL, Liu TD, Zhong ZQ et al (2022) Direct differentiation of human embryonic stem cells to 3D functional hepatocyte-like cells in alginate microencapsulation sphere. Cells 11(19):3134. https://doi.org/10.3390/cells11193134
Xue W, Liu B, Zhang HP, Ryu S et al (2022) Controllable fabrication of alginate/poly-L-ornithine polyelectrolyte complex hydrogel networks as therapeutic drug and cell carriers. Acta Biomater 138:182–192. https://doi.org/10.1016/j.actbio.2021.11.004
Yu SL, Han BS, Peng CH (2012) A preliminary study of alginate, Heparin-Chitosan-Alginate and Heparin microencapsulated hepatocytes system. Hepatogastroenterology 59(116):1234–1240. https://doi.org/10.5754/hge11638
Zakaria L, Wong TW, Anuar NK, Naharudin I, Tripathy M, Sheshala R, Hussain Z (2019) Enhancing sustained drug release property of chitosan in spheroids through crosslinking reaction and coacervation. Powder Technol 354:815–821. https://doi.org/10.1016/j.powtec.2019.07.006
Zhang Y, Cremer PS (2006) Interactions between macromolecules and ions: the Hofmeister series. Curr Opin Chem Biol 10(6):658–663. https://doi.org/10.1016/j.cbpa.2006.09.020
Zhang WJ, Choi JK, He XM (2017) Engineering microvascularized 3D tissue using Alginate-Chitosan microcapsules. J Biomater Tissue Eng 7(2):170–173. https://doi.org/10.1166/jbt.2017.1547
Zhang YH, Lu J, Li ZH, Zhu DH, Yu XP, Li LJ (2021) Enhanced cellular functions of hepatocytes in the hyaluronate-alginate-chitosan microcapsules. Int J Artif Organs 44(5):340–349. https://doi.org/10.1177/0391398820959345
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This work was supported by the Science and Technology Plan Project of Taizhou (2003gy16).
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Chen, L., Jiang, F., Xu, H. et al. Improved membrane stability of alginate-chitosan microcapsules by crosslinking with tannic acid. Biotechnol Lett 45, 1039–1052 (2023). https://doi.org/10.1007/s10529-023-03399-3
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DOI: https://doi.org/10.1007/s10529-023-03399-3