Ca-Alginate Hydrogel with Immobilized Callus Cells as a New Delivery System of Grape Seed Extract
Abstract
:1. Introduction
2. Results and Discussion
2.1. Characterization of Hydrogels Formed from Alginate and Cells of Different Callus Cultures
2.2. Fourier Transform Infrared Analyses (FTIR)
2.3. Thermogravimetric Analysis (TGA) and Diffraction Scanning Calorimetry (DSC)
2.4. Swelling Behavior of GSE-Loaded Alginate Hydrogels with Immobilized Callus Cells
2.5. The Release of GSE from Alginate Hydrogels with Immobilized Callus Cells
3. Conclusions
4. Materials and Methods
4.1. Materials
4.2. Callus Culture Cultivation
4.3. Development of Hydrogels and Their Characterization
4.4. FTIR of GSE-Loaded Ca-Alginate and Alginate/Callus Particles
4.5. The DSC and TGA Analysis
4.6. Texture Analysis
4.7. Swelling Study of Alginate Hydrogels with Immobilized Callus Cells
4.8. Calculation of Encapsulation Efficiency
4.9. The GSE Release In Vitro
4.10. Statistical Analysis
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Durazzo, A.; Lucarini, M. Extractable and non-extractable antioxidants. Molecules 2019, 24, 1933. [Google Scholar] [CrossRef] [Green Version]
- Zou, Y.-C.; Wu, C.-L.; Ma, C.-F.; He, S.; Brennand, C.S.; Yuan, Y. Interactions of grape seed procyanidins with soy protein isolate: Contributing antioxidant and stability properties. LWT-Food Sci. Technol. 2019, 115, 108465. [Google Scholar] [CrossRef]
- Unusan, N. Proanthocyanidins in grape seeds: An updated review of their health benefits and potential uses in the food industry. J. Funct. Foods 2020, 67, 103861–103873. [Google Scholar] [CrossRef]
- Shi, J.; Yu, J.; Pohorly, J.E.; Kakuda, Y. Polyphenolics in grape seeds-biochemistry and functionality. J. Med. Food 2003, 6, 291–299. [Google Scholar] [CrossRef]
- Chedea, V.S.; Braicu, C.; Socaciu, C. Antioxidant/prooxidant activity of a polyphenolic grape seed extract. Food Chem. 2010, 121, 132–139. [Google Scholar] [CrossRef]
- Wang, H.; Xue, Y.; Zhang, H.; Huang, Y.; Yang, G.; Du, M.; Zhu, M.J. Dietary grape seed extract ameliorates symptoms of inflammatory bowel disease in IL 10-deficient mice. Mol. Nutr. Food Res. 2013, 57, 2253–2257. [Google Scholar] [CrossRef] [Green Version]
- Bibi, S.; Kang, Y.; Yang, G.; Zhu, M.-J. Grape seed extract improves small intestinal health through suppressing inflammation and regulating alkaline phosphatase in IL-10-deficient mice. J. Funct. Foods 2016, 20, 245–252. [Google Scholar] [CrossRef]
- Manca, M.L.; Casula, E.; Marongiu, F.; Bacchetta, G.; Sarais, G.; Zaru, M.; Escribano-Ferrer, E.; Peris, J.E.; Usach, I.; Fais, S.; et al. From waste to health: Sustainable exploitation of grape pomace seed extract to manufacture antioxidant, regenerative and prebiotic nanovesicles within circular economy. Sci. Rep. 2020, 10, 14184–14199. [Google Scholar]
- Goodrich, K.M.; Smithson, A.T.; Ickes, A.K.; Neilson, A.P. Pan-colonic pharmacokinetics of catechins and procyanidins in male Sprague–Dawley rats. J. Nutr. Biochem. 2015, 26, 1007–1014. [Google Scholar] [CrossRef]
- Fernández, K.; Roeckel, M.; Canales, E.; Dumont, J. Modeling of the nnanoparticles absorption under a gastrointestinal simulated ambient condition. AAPS PharmSciTech. 2017, 18, 2691–2701. [Google Scholar] [CrossRef]
- Fernandez, K.F.; Gonzalez, M.A.; Parada, M.S. Transport of biodegradable polymeric particles loaded with grape seed extract across Caco-2 cell monolayers. Int. J. Food Sci. Technol. 2018, 53, 794–803. [Google Scholar] [CrossRef]
- Alkhader, E.; Billa, N.; Roberts, C.J. Mucoadhesive chitosan-pectinate nanoparticles for the delivery of curcumin to the colon. AAPS PharmSciTech. 2017, 18, 1009–1018. [Google Scholar] [CrossRef]
- Tang, D.-W.; Yu, S.-H.; Ho, Y.-C.; Huang, B.-Q.; Tsai, G.-J.; Hsieh, H.-Y.; Sung, H.-W.; Mi, F.-L. Characterization of tea catechins-loaded nanoparticles prepared from chitosan and an edible polypeptide. Food Hydrocoll. 2013, 30, 33–41. [Google Scholar] [CrossRef]
- Li, Z.; Gu, L. Fabrication of self-assembled (-)-epigallocatechin gallate (EGCG) ovalbumin–dextran conjugate nanoparticles and their transport across monolayers of human intestinal epithelial Caco-2 cells. J. Agric. Food Chem. 2014, 62, 1301–1309. [Google Scholar] [CrossRef]
- Wang, H.; Gong, X.; Guo, X.; Liu, C.; Fan, Y.-Y.; Zhang, J.; Niu, B.; Li, W. Characterization, release, and antioxidant activity of curcumin-loaded sodium alginate/ZnO hydrogel beads. Int. J. Biol. Macromol. 2019, 121, 1118–1125. [Google Scholar] [CrossRef]
- Li, Z.; Ha, J.; Zou, T.; Gu, L. Fabrication of coated bovine serum albumin (BSA)-epigallocatechin gallate (EGCG) nanoparticles and their transport across monolayers of human intestinal epithelial Caco-2 cells. Food Funct. 2014, 5, 1278–1285. [Google Scholar] [CrossRef]
- Chen, K.; Zhang, H. Alginate/pectin aerogel microspheres for controlled release of proanthocyanidins. Int. J. Biol. Macromol. 2019, 136, 936–943. [Google Scholar] [CrossRef]
- Sheng, K.; Zhang, G.; Kong, X.; Wang, J.; Mu, W.; Wang, Y. Encapsulation and characterisation of grape seed proanthocyanidin extract using sodium alginate and different cellulose derivatives. Int. J. Food Sci. Technol. 2021, 56, 6420–6430. [Google Scholar] [CrossRef]
- Tie, S.; Su, W.; Zhang, X.; Chen, Y.; Zhao, X.; Tan, M. pH-Responsive core-shell microparticles prepared by a microfluidic chip for the encapsulation and controlled release of procyanidins. J. Agric. Food Chem. 2021, 69, 1466–1477. [Google Scholar] [CrossRef]
- Chen, R.; Guo, X.; Liu, X.; Cui, H.; Wang, R.; Han, J. Formulation and statistical optimization of gastric floating alginate/oil/chitosan capsules loading procyanidins: In vitro and in vivo evaluations. Int. J. Biol. Macromol. 2018, 108, 1082–1091. [Google Scholar] [CrossRef]
- Priyadarshi, R.; Riahi, Z.; Rhim, J.-W. Antioxidant pectin/pullulan edible coating incorporated with Vitis vinifera grape seed extract for extending the shelf life of peanuts. Postharv. Biol. Technol. 2022, 183, 111740. [Google Scholar] [CrossRef]
- Muñoz, V.; Kappes, T.; Roeckel, M.; Vera, J.C.; Fernández, K. Modification of chitosan to deliver grapes proanthocyanidins: Physicochemical and biological evaluation. LWT-Food Sci. Technol. 2016, 73, 640–648. [Google Scholar] [CrossRef]
- Yu, H.-L.; Feng, Z.-Q.; Zhang, J.-J.; Wang, Y.-H.; Ding, D.-J.; Gao, Y.-Y.; Zhang, W.-F. The evaluation of proanthocyanidins/chitosan/lecithin microspheres as sustained drug delivery system. BioMed Res. Int. 2018, 2018, 9073420. [Google Scholar] [CrossRef] [Green Version]
- Liu, K.; Feng, Z.; Shan, L.; Yang, T.; Qin, M.; Tang, J.; Zhang, W. Preparation, characterization, and antioxidative activity of Bletilla striata polysaccharide/chitosan microspheres for oligomeric proanthocyanidins. Dry. Technol. 2017, 35, 1629–1643. [Google Scholar] [CrossRef]
- Flamminii, F.; Di Mattia, C.D.; Nardella, M.; Chiarini, M.; Valbonetti, L.; Neri, L.; Difonzo, G.; Pittia, P. Structuring alginate beads with different biopolymers for the development of functional ingredients loaded with olive leaves phenolic extract. Food Hydrocoll. 2020, 108, 105849. [Google Scholar] [CrossRef]
- Basanta, M.F.; Rojas, A.M.; Martinefski, M.R.; Tripodi, V.P.; De’Nobili, M.D.; Fissore, E.N. Cherry (Prunus avium) phenolic compounds for antioxidant preservation at food interfaces. J. Food Eng. 2018, 239, 15–25. [Google Scholar] [CrossRef]
- Fang, Y.; Al-Assaf, S.; Phillips, G.O.; Nishinari, K.; Funami, T.; Williams, P.A. Binding behavior of calcium to polyuronates: Comparison of pectin with alginate. Carbohydr. Polym. 2008, 72, 334–341. [Google Scholar] [CrossRef]
- Paques, J.P.; van der Linden, E.; van Rijn, C.J.M.; Sagis, L.M.C. Preparation methods of alginate nanoparticles. Adv. Colloid. Interface. Sci. 2014, 209, 163–171. [Google Scholar] [CrossRef]
- Gonçalves, V.S.S.; Gurikov, P.; Poejo, J.; Matias, A.A.; Heinrich, S.; Duarte, C.M.M.; Smirnova, I. Alginate-based hybrid aerogel microparticles for mucosal drug delivery. Eur. J. Pharm. Biopharm. 2016, 107, 160–170. [Google Scholar] [CrossRef]
- Seidel, J.; Ahlfeld, T.; Adolph, M.; Kümmritz, S.; Steingroewer, J.; Krujatz, F.; Bley, T.; Gelinsky, M.; Lode, A. Green bioprinting: Extrusion-based fabrication of plant cell-laden biopolymer hydrogel scaffolds. Biofabrication 2017, 9, 045011–045023. [Google Scholar] [CrossRef]
- Vancauwenberghe, V.; Baiye Mfortaw Mbong, V.; Vanstreels, E.; Verboven, P.; Lammertyn, J.; Nicolai, B. 3D printing of plant tissue for innovative food manufacturing: Encapsulation of alive plant cells into pectin based bio-ink. J. Food Eng. 2019, 263, 454–464. [Google Scholar] [CrossRef]
- Park, S.M.; Kim, H.W.; Park, H.J. Callus-based 3D printing for food exemplified with carrot tissues and its potential for innovative food production. J. Food Eng. 2020, 271, 109781–109788. [Google Scholar] [CrossRef]
- Varma, A.; Gemeda, H.B.; McNulty, M.J.; McDonald, K.A.; Nandi, S.; Knipe, J.M. Immobilization of transgenic plant cells towards bioprinting for production of a recombinant biodefense agent. Biotechnol. J. 2021, 16, 2100133. [Google Scholar] [CrossRef] [PubMed]
- Landerneau, S.; Lemarié, L.; Marquette, C.; Petiot, E. Green 3D bioprinting of plant cells: A new scope for 3D bioprinting. Bioprinting 2022, 27, e00216. [Google Scholar] [CrossRef]
- Nordlund, E.; Lille, M.; Silventoinen, P.; Nygren, H.; Seppänen-Laakso, T.; Mikkelson, A.; Aura, A.-M.; Heiniö, R.-L.; Nohynek, L.; Puupponen-Pimiä, R.; et al. Plant cells as food—A concept taking shape. Food Res. Int. 2018, 107, 297–305. [Google Scholar] [CrossRef] [PubMed]
- Belova, K.; Dushina, E.; Popov, S.; Zlobin, A.; Martinson, E.; Vityazev, F.; Litvinets, S. Enrichment of 3D-printed k-carrageenan food gel with callus tissue of narrow-leaved lupin Lupinus angustifolius. Gels 2023, 9, 45. [Google Scholar] [CrossRef]
- Benfattoum, K.; Haddadine, N.; Bouslah, N.; Benaboura, A.; Maincent, P.; Barillé, R.; Sapin-Minet, A.; El-Shall, M.S. Formulation characterization and in vitro evaluation of acacia gum-calcium alginate beads for oral drug delivery systems. Polym. Adv. Technol. 2017, 29, 884–895. [Google Scholar] [CrossRef]
- Awasthi, R.; Kulkarni, G.T.; Ramana, M.V.; de Jesus Andreoli Pinto, T.; Kikuchi, I.S.; Dal Molim Ghisleni, D.; de Souza Braga, M.; De Bank, P.; Dua, K. Dual crosslinked pectin-alginate network as sustained release hydrophilic matrix for repaglinide. Int. J. Biol. Macromol. 2017, 97, 721–732. [Google Scholar] [CrossRef] [Green Version]
- Aquino, R.P.; Auriemma, G.; D’Amore, M.; D’Ursi, A.M.; Mencherini, T.; Del Gaudio, P. Piroxicam loaded alginate beads obtained by prilling/microwave tandem technique: Morphology and drug release. Carbohydr. Polym. 2012, 223, 740–748. [Google Scholar] [CrossRef]
- Günter, E.A.; Popeyko, O.V. Delivery system for grape seed extract based on biodegradable pectin-Zn-alginate gel particles. Int. J. Biol. Macromol. 2022, 219, 1021–1033. [Google Scholar] [CrossRef]
- Roh, Y.H.; Shin, C.S. Preparation and characterization of alginate-carrageenan complex films. J. Appl. Polym. Sci. 2006, 99, 3483–3490. [Google Scholar] [CrossRef]
- De Souza, V.B.; Thomazini, M.; Echalar Barrientos, M.A.; Nalin, C.M.; Ferro-Furtado, R.; Genovese, M.I.; Favaro-Trindade, C.S. Functional properties and encapsulation of a proanthocyanidin-rich cinnamon extract (Cinnamomum zeylanicum) by complex coacervation using gelatin and different polysaccharides. Food Hydrocoll. 2018, 77, 297–306. [Google Scholar] [CrossRef]
- Belščak-Cvitanović, A.; Komes, D.; Karlović, S.; Djaković, S.; Špoljarić, I.; Mršić, G.; Ježek, D. Improving the controlled delivery formulations of caffeine in alginate hydrogel beads combined with pectin, carrageenan, chitosan and psyllium. Food Chem. 2015, 167, 378–386. [Google Scholar] [CrossRef] [PubMed]
- Khaksar, R.; Hosseini, S.M.; Hosseini, H.; Shojaee-Aliabadi, S.; Mohammadifar, M.A.; Mortazavian, A.M.; Javadi, N.H.S.; Komeily, R. Nisin-loaded alginate-high methoxy pectin microparticles: Preparation and physicochemical characterization. Int. J. Food Sci. Technol. 2014, 49, 2076–2082. [Google Scholar] [CrossRef]
- Arab, M.; Hosseini, S.M.; Nayebzadeh, K.; Khorshidian, N.; Yousefi, M.; Razavi, S.H.; Mortazavian, A.M. Microencapsulation of microbial canthaxanthin with alginate and high methoxyl pectin and evaluation the release properties in neutral and acidic condition. Int. J. Biol. Macromol. 2019, 121, 691–698. [Google Scholar] [CrossRef]
- Duan, H.; Lü, S.; Qin, H.; Gao, C.; Bai, X.; Wei, Y.; Wu, X.; Liu, M.; Zhang, X.; Liu, Z. Co-delivery of zinc and 5-aminosalicylic acid from alginate/N-succinyl-chitosan blend microspheres for synergistic therapy of colitis. Int. J. Pharm. 2017, 516, 214–224. [Google Scholar] [CrossRef]
- Fu, C.; Yang, D.; Peh, W.Y.E.; Lai, S.; Feng, X.; Yang, H. Structure and antioxidant activities of proanthocyanidins from elephant apple (Dillenia indica Linn. ). J. Food Sci. 2015, 80, 2191–2199. [Google Scholar] [CrossRef]
- De Freitas, E.D.; Lima, B.M.; Rosa, P.C.P.; da Silva, M.G.C.; Vieira, M.G.A. Evaluation of proanthocyanidin-crosslinked sericin/alginate blend for ketoprofen extended release. Adv. Powder Technol. 2019, 30, 1531–1543. [Google Scholar] [CrossRef]
- Rayment, P.; Wright, P.; Hoad, C.; Ciampi, E.; Haydock, D.; Gowland, P.; Butler, M.F. Investigation of alginate beads for gastro-intestinal functionality, Part 1: In vitro characterization. Food Hydrocoll. 2009, 23, 816–822. [Google Scholar] [CrossRef]
- Murashige, T.; Skoog, S.A. Revised medium for rapid growth and bioassays with tobaco tissue cultures. Physiol. Plant. 1962, 15, 473–479. [Google Scholar] [CrossRef]
- Chang, K.L.B.; Lin, J. Swelling behavior and the release of protein from chitosan-pectin composite particles. Carbohydr. Polym. 2000, 43, 163–169. [Google Scholar] [CrossRef]
- Gebara, C.; Chaves, K.S.; Ribeiro, M.C.E.; Souza, F.N.; Grosso, C.R.F.; Gigante, M.L. Viability of Lactobacillus acidophilus La5 in pectin-whey protein microparticles during exposure to simulated gastrointestinal conditions. Food Res. Int. 2013, 51, 872–878. [Google Scholar] [CrossRef] [Green Version]
- Günter, E.A.; Popeyko, O.V. Calcium pectinate gel beads obtained from callus cultures pectins as promising systems for colon-targeted drug delivery. Carbohydr. Polym. 2016, 147, 490–499. [Google Scholar] [CrossRef] [PubMed]
Gel Formulation | Content of Callus Cells (g/mL) | Concentration of Alginate (%) | Diameter of Particles (mm) | Encapsulation Efficiency (%) |
---|---|---|---|---|
Alg0.5 | 0 | 0.5 | 3.303 ± 0.132 | 48.3 ± 0.2 |
0.17SVC-0.5Alg | 0.17 | 0.5 | 3.759 ± 0.095 a | 63.6 ± 0.6 a |
0.33SVC-0.5Alg | 0.33 | 0.5 | 3.907 ± 0.124 a | 67.8 ± 0.5 a |
0.5SVC-0.5Alg | 0.50 | 0.5 | 4.056 ± 0.152 a | 65.8 ± 1.0 a |
0.17LMC-0.5Alg | 0.17 | 0.5 | 3.688 ± 0.132 a | 72.4 ± 0.4 a |
0.33LMC-0.5Alg | 0.33 | 0.5 | 3.811 ± 0.143 a | 68.9 ± 0.5 a |
0.5LMC-0.5Alg | 0.50 | 0.5 | 3.933 ± 0.154 a | 65.5 ± 0.5 a |
Alg1.0 | 0 | 1.0 | 3.631 ± 0.122 a | 50.7 ± 1.0 a |
0.17SVC-1.0Alg | 0.17 | 1.0 | 4.036 ± 0.143 a,b | 71.6 ± 0.3 a,b |
0.33SVC-1.0Alg | 0.33 | 1.0 | 4.231 ± 0.161 a,b | 76.5 ± 0.3 a,b |
0.5SVC-1.0Alg | 0.50 | 1.0 | 4.425 ± 0.178 a,b | 72.9 ± 0.3 a,b |
0.17LMC-1.0Alg | 0.17 | 1.0 | 3.806 ± 0.152 a,b | 76.3 ± 0.5 a,b |
0.33LMC-1.0Alg | 0.33 | 1.0 | 4.044 ± 0.128 a,b | 72.8 ± 0.4 a,b |
0.5LMC-1.0Alg | 0.50 | 1.0 | 4.282 ± 0.104 a,b | 64.7 ± 0.3 a,b |
Gel Formulation | Initial Gel Strength (N) | Work (N·s) | Adhesiveness (N) | Elasticity (mm) |
---|---|---|---|---|
Alg0.5 | 0.472 ± 0.059 | 0.284 ± 0.034 | 0.020 ± 0.001 | 1.938 ± 0.075 |
0.17SVC-0.5Alg | 0.246 ± 0.028 a | 0.192 ± 0.027 a | 0.019 ± 0.001 a | 1.977 ± 0.113 |
0.33SVC-0.5Alg | 0.282 ± 0.020 a | 0.265 ± 0.039 | 0.019 ± 0.001 a | 2.329 ± 0.208 a |
0.5SVC-0.5Alg | 0.244 ± 0.019 a | 0.242 ± 0.027 a | 0.018 ± 0.001 a | 2.362 ± 0.187 a |
0.17LMC-0.5Alg | 0.358 ± 0.058 a | 0.251 ± 0.037 a | 0.018 ± 0.001 a | 1.992 ± 0.058 a |
0.33LMC-0.5Alg | 0.260 ± 0.030 a | 0.251 ± 0.052 a | 0.018 ± 0.001 a | 2.225 ± 0.196 a |
0.5LMC-0.5Alg | 0.211 ± 0.017 a | 0.377 ± 0.039 a | 0.018 ± 0.001 a | 2.351 ± 0.326 a |
Alg1.0 | 1.228 ± 0.086 a | 0.942 ± 0.079 a | 0.019 ± 0.004 | 2.678 ± 0.169 a |
0.17SVC-1.0Alg | 0.654 ± 0.096 a,b | 0.626 ± 0.080 a,b | 0.018 ± 0.001 a | 2.679 ± 0.188 a |
0.33SVC-1.0Alg | 0.670 ± 0.050 a,b | 0.678 ± 0.064 a,b | 0.017 ± 0.001 a | 2.709 ± 0.176 a |
0.5SVC-1.0Alg | 0.575 ± 0.048 a,b | 0.537 ± 0.074 a,b | 0.016 ± 0.001 a,b | 2.607 ± 0.139 a |
0.17LMC-1.0Alg | 0.808 ± 0.100 a,b | 0.761 ± 0.101 a,b | 0.017 ± 0.001 a | 2.776 ± 0.160 a |
0.33LMC-1.0Alg | 0.715 ± 0.090 a,b | 0.789 ± 0.136 a,b | 0.016 ± 0.002 a,b | 2.829 ± 0.155 a,b |
0.5LMC-1.0Alg | 0.558 ± 0.058 a,b | 0.574 ± 0.068 a,b | 0.016 ± 0.002 a,b | 2.618 ± 0.166 a |
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Günter, E.; Popeyko, O.; Popov, S. Ca-Alginate Hydrogel with Immobilized Callus Cells as a New Delivery System of Grape Seed Extract. Gels 2023, 9, 256. https://doi.org/10.3390/gels9030256
Günter E, Popeyko O, Popov S. Ca-Alginate Hydrogel with Immobilized Callus Cells as a New Delivery System of Grape Seed Extract. Gels. 2023; 9(3):256. https://doi.org/10.3390/gels9030256
Chicago/Turabian StyleGünter, Elena, Oxana Popeyko, and Sergey Popov. 2023. "Ca-Alginate Hydrogel with Immobilized Callus Cells as a New Delivery System of Grape Seed Extract" Gels 9, no. 3: 256. https://doi.org/10.3390/gels9030256