Food and Bioprocess Technology

, Volume 11, Issue 5, pp 1050–1060 | Cite as

Construction of a Biocompatible and Antioxidant Multilayer Coating by Layer-by-Layer Assembly of κ-Carrageenan and Quercetin Nanoparticles

  • Marthyna P. Souza
  • Antônio F. M. Vaz
  • Thacianna B. Costa
  • Miguel A. Cerqueira
  • Célia M. M. B. De Castro
  • António A. Vicente
  • Maria G. Carneiro-da-Cunha
Original Paper
  • 53 Downloads

Abstract

The present work aimed at the construction and characterization of a multilayer coating based on κ-carrageenan and quercetin-loaded lecithin/chitosan nanoparticles (Np) by the layer-by-layer technique and the evaluation of its antioxidant capacity and potential cytotoxicity in vitro. The multilayered coating was successfully self-assembled, as confirmed by UV-Vis spectroscopy, contact angle, atomic force microscopy (AFM), and scanning electron microscopy (SEM). Multilayered coatings showed to have antioxidant capacity, with a DPPH• radical scavenging activity of 31.32 ± 3.13% and a result of the FRAP assay of 799.41 ± 95.39 μM of ferrous ion (Fe2+) equivalent. These coatings were also shown to be devoid of cell toxicity, as evaluated by determination of nitric oxide production and 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide (MTT) test. The alveolar macrophages culture was tested in the presence of the κ-carrageenan/quercetin-Np multilayer coating and showed a cell viability of 91.3 ± 9.6%. These results suggest that this multilayered coating is adequate for surfaces modification in view of biomedical and food industry applications.

Keywords

Biomaterial Cytotoxicity Multilayer Polyelectrolyte Surface modification 

Notes

Acknowledgements

This work was supported by the Portuguese Foundation for Science and Technology (FCT) under the scope of the strategic funding of UID/BIO/04469/2013 unit, and COMPETE 2020 (POCI-01-0145-FEDER-006684) and BioTecNorte operation (NORTE-01-0145-FEDER-000004) funded by the European Regional Development Fund under the scope of Norte2020 - Programa Operacional Regional do Norte. The authors would also like to thank the Brazilian Government for support given by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). Carneiro-da-Cunha, M.G. expresses her gratitude to the CNPq for research grant.

References

  1. Albuquerque, P. B. S., Coelho, L. C. B. B., Teixeira, J. A., & Carneiro-da-Cunha, M. G. (2016). Approaches in biotechnological applications of natural polymers. AIMS Molecular Science, 3(3), 386–425.  https://doi.org/10.3934/molsci.2016.3.386.CrossRefGoogle Scholar
  2. Barbosa, K. B. F., Costa, N. M. B., Alfenas, R. C. G., De Paula, S. O., Minim, V. P. R., & Bressan, J. (2010). Oxidative stress: concept, implications and modulating factors. Brazilian Jornal of Nutrition, 23(4), 629–643.Google Scholar
  3. Bastarrachea, L. J., Wong, D. E., Roman, M. J., Lin, Z., & Goddard, J. M. (2015). Active packaging coatings. Coatings, 5, 771–791.CrossRefGoogle Scholar
  4. Busolo, M. A., & Lagaron, J. M. (2015). Antioxidant polyethylene films based on a resveratrol containing clay of interest in food packaging applications. Food Packaging and Shelf Life, 6, 30–41.  https://doi.org/10.1016/j.fpsl.2015.08.004.CrossRefGoogle Scholar
  5. Carneiro-da-Cunha, M. G., Cerqueira, M. A., Souza, B. W. S., Carvalho, S., Quintas, M. A. C., Teixeira, J. A., et al. (2010). Physical and thermal properties of a chitosan/alginate nanolayered PET film. Carbohydrate Polymers, 82(1), 153–159.  https://doi.org/10.1016/j.carbpol.2010.04.043.CrossRefGoogle Scholar
  6. Carrizo, D., Taborda, G., Nerín, C., & Bosetti, O. (2016). Extension of shelf life of two fatty foods using a new antioxidante multilayer packaging containing green tea extract. Innovative Food Science and Emerging Technologies, 33, 534–541.  https://doi.org/10.1016/j.ifset.2015.10.018.CrossRefGoogle Scholar
  7. Chen, W., Shen, X., Hu, H., Xu, K., Ran, Q., Yu, Y., et al. (2017). Surface functionalization of titanium implants with chitosan-catechol conjugate for suppression of ROS-induced cells damage and improvement of osteogenesis. Biomaterials, 114, 82–96.  https://doi.org/10.1016/j.biomaterials.2016.10.055.CrossRefGoogle Scholar
  8. De Castro, C. M. M. B., Nahori, M. A., Dumarey, C. H., Vargaftig, B. B., & Bachelet, M. (1995). Fenspiride: an anti-inflammatory drug with potential benefits in the treatment of endotoxemia. European Journal of Pharmacology, 294(2-3), 669–676.  https://doi.org/10.1016/0014-2999(95)00608-7.CrossRefGoogle Scholar
  9. Ebrahimiasl, S., Zakaria, A., Kassim, A., & Basri, S. N. (2015). Novel conductive polypyrrole/zinc oxide/chitosan bionanocomposite: synthesis, characterization, antioxidant, and antibacterial activities. International Journal of Nanomedicine, 10, 217–227.  https://doi.org/10.2147/IJN.S69740.Google Scholar
  10. Fabra, M. J., Flores-López, M. L., Cerqueira, M. A., Rodriguez, D. J., Lagaron, J. M., & Vicente, A. A. (2016). Layer-by-layer technique to developing functional nanolaminate films with antifungal activity. Food and Bioprocess Technology, 9(3), 471–480.  https://doi.org/10.1007/s11947-015-1646-1.CrossRefGoogle Scholar
  11. Feder, L. S., & Laskin, D. L. (1994). Regulation of hepatic endothelial cell and macrophage proliferation and nitric oxide production by GM-CSF, M-CSF, and lL-13 following acute endotoxemia. Journal of Leukocyte Biology, 55(4), 507–513.  https://doi.org/10.1002/jlb.55.4.507.CrossRefGoogle Scholar
  12. Fu, J., Ji, J., Yuan, W., & Shen, J. (2005). Construction of anti-adhesive and antibacterial multilayer films via layer-by-layer assembly of heparin and chitosan. Biomaterials, 26(33), 6684–6692.  https://doi.org/10.1016/j.biomaterials.2005.04.034.CrossRefGoogle Scholar
  13. Gadelmawla, E. S., Koura, M. M., Maksoud, T. M. A., Elewa, I. M., & Soliman, H. H. (2002). Roughness parameters. Journal of Materials Processing Technology, 123(1), 133–145.  https://doi.org/10.1016/S0924-0136(02)00060-2.CrossRefGoogle Scholar
  14. Gand, A., Hindié, M., Chacon, D., Tassel, P. R. V., & Pauthe, E. (2014). Nanotemplated polyelectrolyte films as porous biomolecular delivery systems. Biomatter, 4(1), e28823.  https://doi.org/10.4161/biom.28823.CrossRefGoogle Scholar
  15. Guzmán, E., Mateos-Maroto, A., Ruano, M., Ortega, F., & Rubio, R. G. (2017). Layer-by-layer polyelectrolyte assemblies for encapsulation and release of active compounds. Advances in Colloid and Interface Science, 249, 290–307.  https://doi.org/10.1016/j.cis.2017.04.009.CrossRefGoogle Scholar
  16. ISO 10993-5. (2009). International standard for biological evaluation of medical devices––part 5: tests for in vitro cytotoxicity.Google Scholar
  17. Jones, O., Decker, E. A., & McClements, D. J. (2010). Thermal analysis of β-lactoglobulin complexes with pectins or carrageenan for production of stable biopolymer particles. Food Hydrocolloids, 24(2-3), 239–248.  https://doi.org/10.1016/j.foodhyd.2009.10.001.CrossRefGoogle Scholar
  18. Kao, W. J. (1999). Evaluation of protein-modulated macrophage behavior on biomaterials: designing biomimetic materials for cellular engineering. Biomaterials, 20(23–24), 2213–2221.  https://doi.org/10.1016/S0142-9612(99)00152-0.CrossRefGoogle Scholar
  19. Kononova, S. V., Volod’ko, A. V., Petrova, V. A., Kruchinina, E. V., Baklagina, Y. G., Chusovitin, E. A., & Skorik, Y. A. (2018). Pervaporation multilayer membranes based on a polyelectrolyte complex of λ-carrageenan and chitosan. Carbohydrate Polymers, 181, 86–92.  https://doi.org/10.1016/j.carbpol.2017.10.050.CrossRefGoogle Scholar
  20. Limpisophon, K., & Schleining, G. (2017). Use of gallic acid to enhance the antioxidant and mechanical properties of active fish gelatin film. Journal of Food Science, 82(1), 80–89.  https://doi.org/10.1111/1750-3841.13578.CrossRefGoogle Scholar
  21. Lith, R. V., Gregory, E. K., Yang, J., Kibbe, M. R., & Ameer, G. A. (2014). Engineering biodegradable polyester elastomers with antioxidante properties to attenuate oxidative stress in tissues. Biomaterials, 35(28), 8113–8122.  https://doi.org/10.1016/j.biomaterials.2014.06.004.CrossRefGoogle Scholar
  22. Liu, S., & Li, L. (2016). Thermoreversible gelation and scaling behavior of Ca2+-induced κ-carrageenan hydrogels. Food Hydrocolloids, 61, 793–800.  https://doi.org/10.1016/j.foodhyd.2016.07.003.CrossRefGoogle Scholar
  23. Liu, Y., He, T., & Gao, C. (2005). Surface modification of poly(ethylene terephthalate) via hydrolysis and layer-by-layer assembly of chitosan and chondroitin sulfate to constructo cytocompatible layer for human endothelial cells. Colloids and Surfaces B: Biointerfaces, 46(2), 117–126.  https://doi.org/10.1016/j.colsurfb.2005.09.005.CrossRefGoogle Scholar
  24. Liu, Q., Wu, J., Lim, Z. Y., Aggarwal, A., Yang, H., & Wang, S. (2017). Evaluation of the metabolic response of Escherichia coli to electrolysed water by 1H NMR spectroscopy. LWT - Food Science and Technology, 79, 428–436.  https://doi.org/10.1016/j.lwt.2017.01.066.CrossRefGoogle Scholar
  25. Manzocco, L., Valoppi, F., Calligaris, S., Andreatta, F., Spilimbergo, S., & Nicoli, M. C. (2017). Exploitation of κ-carrageenan aerogels as template for edible oleogel preparation. Food Hydrocolloids, 71, 68–75.  https://doi.org/10.1016/j.foodhyd.2017.04.021.CrossRefGoogle Scholar
  26. Medeiros, B. G. S., Pinheiro, A. C., Teixeira, J. A., Vicente, A. A., & Carneiro-da-Cunha, M. G. (2012). Polysaccharide/protein nanomultilayer coatings: construction, characterization and evaluation of their effect on ‘Rocha’ pear (Pyrus communis L.) shelf-life. Food and Bioprocess Technology, 5(6), 2435–2445.  https://doi.org/10.1007/s11947-010-0508-0.CrossRefGoogle Scholar
  27. Medeiros, B. G. S., Souza, M. P., Pinheiro, A. C., Bourbon, A. I., Cerqueira, M. A., Vicente, A. A., & Carneiro-da-Cunha, M. G. (2014). Physical characterisation of an alginate/lysozyme nanolaminate coating and its evaluation on ‘Coalho’ cheese shelf life. Food and Bioprocess Technology, 7(4), 1088–1098.  https://doi.org/10.1007/s11947-013-1097-5.CrossRefGoogle Scholar
  28. Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assay. Journal of lmmunological Methods, 65(1-2), 55–63.  https://doi.org/10.1016/0022-1759(83)90303-4.CrossRefGoogle Scholar
  29. Necas, J., & Bartosikova, L. (2013). Carrageenan: a review. Veterinární Medicína, 58(4), 187–205.CrossRefGoogle Scholar
  30. Newman, A. W., & Kwok, D. Y. (1999). Contact angle measurement and contact angle interpretation. Advances in Colloid and Interface Science, 81(3), 167–249.CrossRefGoogle Scholar
  31. Pauthe, E., & Tassel, P. R. V. (2014). Layer-by-layer films as biomaterials: bioactivity and mechanics. Journal of Biomaterials Science, 25(14-15), 1489–1501.  https://doi.org/10.1080/09205063.2014.921096.CrossRefGoogle Scholar
  32. Peng, L., Li, H., & Meng, Y. (2016). Layer-by-layer structured polysaccharides-based multilayers on cellulose acetate membrane: towards better hemocompatibility, antibacterial and antioxidant activities. Applied Surface Science, 401, 25–39.CrossRefGoogle Scholar
  33. Pinheiro, A. C., Bourbon, A. I., Medeiros, B. G. S., Silva, L. H. M., Silva, M. C. H., Carneiro-da-Cunha, M. G., et al. (2012). Interactions between κ-carrageenan and chitosan in nanolayered coatings-structural and transport properties. Carbohydrate Polymers, 87(2), 1081–1090.  https://doi.org/10.1016/j.carbpol.2011.08.040.CrossRefGoogle Scholar
  34. Russo, M., Spagnuolo, C., Tedesco, I., Bilotto, S., & Russo, G. L. (2012). The flavonoid quercetin in disease prevention and therapy: facts and fancies. Biochemical Pharmacology, 83(1), 6–15.  https://doi.org/10.1016/j.bcp.2011.08.010.CrossRefGoogle Scholar
  35. Souza, M. P., Vaz, A. F. M., Correia, M. T. S., Cerqueira, M. A., Vicente, A. A., & Carneiro-da-Cunha, M. G. (2014). Quercetin-loaded lecithin/chitosan nanoparticles for functional food applications. Food and Bioprocess Technlogy, 7(4), 1149–1159.  https://doi.org/10.1007/s11947-013-1160-2.CrossRefGoogle Scholar
  36. Souza, M. P., Vaz, A. F. M., Cerqueira, M. A., Texeira, J. A., Vicente, A. A., & Carneiro-da-Cunha, M. G. (2015a). Effect of an edible nanomultilayer coating by electrostatic self-assembly on the shelf life of fresh-cut mangoes. Food and Bioprocess Technology, 8(3), 647–654.  https://doi.org/10.1007/s11947-014-1436-1.CrossRefGoogle Scholar
  37. Souza, M. P., Vaz, A. F. M., Silva, H. D., Cerqueira, M. A., Vicente, A. A., & Carneiro-da-Cunha, M. G. (2015b). Development and characterization of an active chitosan-based film containing quercetin. Food and Bioprocess Technlogy, 8(11), 2183–2191.  https://doi.org/10.1007/s11947-015-1580-2.CrossRefGoogle Scholar
  38. Stenner, R., Matubayasi, N., & Shimizu, S. (2016). Gelation of carrageenan: effects of sugars and polyols. Food Hydrocolloids, 54, 284–292.  https://doi.org/10.1016/j.foodhyd.2015.10.007.CrossRefGoogle Scholar
  39. Toledo, C. E. P., Souza, M. A., Fraga, M. R., Ribeiro, L. C., Ferreira, A. P., & Vitral, R. W. F. (2012). Cellular viability and nitric oxide (NO) production by J774 macrophages in the presence of orthodontic archwires. Journal Biomedical Science and Engineering, 5(05), 255–262.  https://doi.org/10.4236/jbise.2012.55032.CrossRefGoogle Scholar
  40. Vera, P., Echegoyen, Y., Canellas, E., Nerín, C., Palomo, M., Madrid, Y., & Cámara, C. (2016). Nano selenium as antioxidant agent in a multilayer food packaging material. Analytical and Bioanalytical Chemistry, 408(24), 6659–6670.  https://doi.org/10.1007/s00216-016-9780-9.CrossRefGoogle Scholar
  41. Xia, Z., & Triffitt, J. T. (2006). A review on macrophage responses to biomaterials. Biomedical Materials, 1, 1–9.CrossRefGoogle Scholar
  42. Yang, Z., Yang, H., & Yang, H. (2018). Effects of sucrose addition on the rheology and microstructure of κ-carrageenan gel. Food Hydrocolloids, 75, 164–173.  https://doi.org/10.1016/j.foodhyd.2017.08.032.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Marthyna P. Souza
    • 1
    • 2
    • 3
  • Antônio F. M. Vaz
    • 4
  • Thacianna B. Costa
    • 2
  • Miguel A. Cerqueira
    • 3
    • 5
  • Célia M. M. B. De Castro
    • 2
  • António A. Vicente
    • 3
  • Maria G. Carneiro-da-Cunha
    • 1
    • 2
  1. 1.Biochemistry DepartmentUniversidade Federal de Pernambuco-UFPERecifeBrazil
  2. 2.LIKA - Laboratório de Imunopatologia Keizo AsamiUFPE, Cidade UniversitariaRecifeBrazil
  3. 3.CEB – Centre of Biological EngineeringUniversidade do MinhoBragaPortugal
  4. 4.Unidade Acadêmica de Medicina VeterináriaUniversidade Federal de Campina GrandePatosBrazil
  5. 5.International Iberian Nanotechnology Laboratory-INLBragaPortugal

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