Controlled Release of Curcumin by Graphene Oxide/Chitosan/Sodium Alginate Hydrogel Multilayer Nanocomposites and Evaluate its Synergistic Antibacterial Activity

Document Type : Research Article

Authors

Department of Biology, Faculty of Sciences, Shahid Bahonar University of Kerman, Kerman, Iran

Abstract

Curcumin has many medical properties, such as anti-inflammatory, anti-microbial, antioxidant, and anti-tumor activities. However, its hydrophobic nature results in less solubility and fast metabolism. Nowadays, designing a cargo based on nano-biotechnology is an efficient method to overcome these limitations of curcumin. This study synthesized graphene oxide/chitosan/sodium alginate (GCA) multilayer nanocomposites according to a layer-by-layer (LBL) assembly to load curcumin. Firstly, for graphene oxide/chitosan (GC) nanocomposite synthesis, graphene oxide (G) suspension was added to the chitosan (CS) solution dropwise during stirring. Then, sodium alginate (A) in water was added to the GC suspension drop wisely, centrifuged, and lyophilized. This GCA multilayer nanocomposite showed a layered structure with negative zeta potential. Though the drug loading efficiency of this GCA multilayer was not as high as graphene oxide, its curcumin release was pH-dependent. The highest drug release belonged to GCA due to the presence of curcumin in the hydrogel network without tight binding. This release was pH-dependent as the curcumin release after 24 h was 80% in pH 5 for GCA, while this amount was 60 % in pH 7 because of hydrogel network disruption in the acidic environment. The antibacterial results exhibited that this GCA multilayer did not show any antibacterial activity. It was significant that curcumin did not affect E. coli, though the minimum inhibitory concentration (MIC) for S. aureus was 300 µg/ml. Ciprofloxacin has been used to investigate the effect of GCA nanocomposite’s synergetic release of curcumin and antibiotics. Results showed that ciprofloxacin increased the inhibition zone diameter for S. aureus, but this was not observed in E. coli. Overall, it can be concluded that the antibacterial activity of curcumin is not evitable. To explain this, the antioxidant activity of curcumin, which reduces the radicals due to ciprofloxacin activity, can be considered.

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Bennis, S., Chapey, C., Robert, J., & Couvreur, P. (1994). Enhanced cytotoxicity of doxorubicin encapsulated in polyisohexylcyanoacrylate nanospheres against multidrug-resistant tumour cells in culture. European Journal of Cancer, 30(1), 89-93. https://doi.org/10.1016/S0959-8049(05)80025-5.
Chidambaram, M., & Krishnasamy, K. (2014). Nanoparticulate drug delivery system to overcome the limitations of conventional curcumin in the treatment of various cancers: a review. Drug Delivery Letters, 4(2), 116-127. https://doi.org/10.2174/2210303103999 131211110708.
Desai, M. P., Labhasetwar, V., Amidon, G. L., & Levy, R. J. (1996). Gastrointestinal uptake of biodegradable microparticles: effect of particle size. Pharmaceutical Research, 13, 1838-1845. https://doi.org/10.1023/A:10160851 08889.
Ghawanmeh, A. A., Ali, G. A., Algarni, H., Sarkar, S. M., & Chong, K. F. (2019). Graphene oxide-based hydrogels as a nanocarrier for anticancer drug delivery. Nano Research, 12, 973-990. https://doi.org/10.1007/s12274-019-2300-4.
Goswami, M., Mangoli, S. H., & Jawali, N. (2006). Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli. Antimicrobial Agents and Chemotherapy, 50(3), 949-954. https://doi.org/10.1128/AAC.50.3.949-954.2006.
Helson, L. (2013). Curcumin (diferuloylmethane) delivery methods: a review. Biofactors, 39(1), 21-26. https://doi.org/10.1002/biof.1080.
Hu, M., & Mi, B. (2014). Layer-by-layer assembly of graphene oxide membranes via electrostatic interaction. Journal of Membrane Science, 469, 80-87. https://doi.org/10.1016/j.memsci.2014.06.036
Hussain, Z., Thu, H. E., Amjad, M. W., Hussain, F., Ahmed, T. A., & Khan, S. (2017). Exploring recent developments to improve antioxidant, anti-inflammatory and antimicrobial efficacy of curcumin: a review of new trends and future perspectives. Materials Science and Engineering: 77, 1316-1326. https://doi.org/10.1016/j.msec.2017.03.226.
Itzia Azucena, R. C., José Roberto, C. L., Martin, Z. R., Rafael, C. Z., Leonardo, H. H., Gabriela, T. P., & Araceli, C. R. (2019). Drug susceptibility testing and synergistic antibacterial activity of curcumin with antibiotics against enterotoxigenic Escherichia coli. Antibiotics, 8(2), 43. https://doi.org/10.3390/antibiotics8020043.
Jalaladdiny, S.S., Badoei-dalfard, A., Karami, Z., & Sargazi, G. (2022) Co-delivery of doxorubicin and curcumin to breast cancer cells by a targeted delivery system based on Ni/Ta core-shell metal-organic framework coated with folic acid-activated chitosan nanoparticles. Journal of the Iranian Chemical Society, 19(10), 4287-4298. https://doi.org/10.1007/s13738-022-02604-w.
Jamil, Q. U. A., Jaerapong, N., Zehl, M., Jarukamjorn, K., & Jäger, W. (2017). Metabolism of curcumin in human breast cancer cells: impact of sulfation on cytotoxicity. Planta Medica, 83, 1028-1034. https://doi.org/10.1055/s-0043-107885.
Kiew, S. F., Kiew, L. V., Lee, H. B., Imae, T., & Chung, L. Y. (2016). Assessing biocompatibility of graphene oxide-based nanocarriers: a review. Journal of Controlled Release, 226, 217-228. https://doi.org/10.1016/j.jconrel.2016.02.015.
Li, L., Zhang, X., Pi, C., Yang, H., Zheng, X., Zhao, L., & Wei, Y. (2020). Review of curcumin physicochemical targeting delivery system. International Journal of Nanomedicine, 15, 9799-9821. https://doi.org/10.2147/IJN.S276201.
Lim, G. P., Chu, T., Yang, F., Beech, W., Frautschy, S. A., & Cole, G. M. (2001). The curry spice curcumin reduces oxidative damage and amyloid pathology in an Alzheimer transgenic mouse. Journal of Neuroscience, 21(21), 8370-8377. https://doi.org/10.1523/JNEUROSCI.21-21-08370.2001.
Ma, Z., Haddadi, A., Molavi, O., Lavasanifar, A., Lai, R., & Samuel, J. (2008). Micelles of poly (ethylene oxide)-b-poly (ε-caprolactone) as vehicles for the solubilization, stabilization, and controlled delivery of curcumin. Journal of Biomedical Materials Research, 86(2), 300-310. https://doi.org/10.1002/jbm.a.31584.
Mehrabi, M., Karami, F., Siah, M., Esmaeili, S., & Khodarahmi, R. (2022). Is curcumin an active suicidal antioxidant only in the aqueous environments? Journal of the Iranian Chemical Society, 19(8), 3441-3450. https://doi.org/10.1007/s13738-022-02538-3.
Mehrabi, M., Esmaeili, S., Ezati, M., Abassi, M., Rasouli, H., Nazari, D., ... & Khodarahmi, R. (2021). Antioxidant and glycohydrolase inhibitory behavior of curcumin-based compounds: synthesis and evaluation of anti-diabetic properties in vitro. Bioorganic Chemistry, 110, 104720. https://doi.org/10.1016/j.bioorg.2021.104720.
Moghaddam, K. M., Iranshahi, M., Yazdi, M. C., & Shahverdi, A. R. (2009). The combination effect of curcumin with different antibiotics against Staphylococcus aureus. International Journal of Green Pharmacy, 3(2), 141-143. https://doi.org/10.4103/0973-8258.54906.
Mu, L., & Feng, S. S. (2003). A novel controlled release formulation for the anticancer drug paclitaxel (Taxol®): PLGA nanoparticles containing vitamin E TPGS. Journal of Controlled Release, 86(1), 33-48. https://doi.org/9780429162640.
Mun, S. H., Joung, D. K., Kim, Y. S., Kang, O. H., Kim, S. B., Seo, Y. S., ... & Kwon, D. Y. (2013). Synergistic antibacterial effect of curcumin against methicillin-resistant Staphylococcus aureus. Phytomedicine, 20(8-9), 714-718. https://doi.org/10.1016/j.phymed.2013.02.006 Nurunnabi, M., Parvez, K., Nafiujjaman, M., Revuri, V., Khan, H. A., Feng, X., & Lee, Y. K. (2015). Bioapplication of graphene oxide derivatives: drug/gene delivery, imaging, polymeric modification, toxicology, therapeutics and challenges. RSC Advances, 5(52), 42141-42161. https://doi.org/10.1039/c5ra04756k.
Pan, Y., Sahoo, N. G., & Li, L. (2012). The application of graphene oxide in drug delivery. Expert Opinion on Drug Delivery, 9(11), 1365-1376. https://doi.org/10.1517/17425247.2012.729575.
Panyam, J., Williams, D., Dash, A., Leslie‐Pelecky, D., & Labhasetwar, V. (2004). Solid‐state solubility influences encapsulation and release of hydrophobic drugs from PLGA/PLA nanoparticles. Journal of Pharmaceutical Sciences, 93(7), 1804-1814. https://doi.org/10.1002/jps.20094.
Raja, M. A., Arif, M., Feng, C., Zeenat, S., & Liu, C. G. (2017). Synthesis and evaluation of pH-sensitive, self-assembled chitosan-based nanoparticles as efficient doxorubicin carriers. Journal of Biomaterials Applications, 31(8), 1182-1195. https://doi.org/10.1177/0885328216681184.
Ramazani, A., Abrvash, M., Sadighian, S., Rostamizadeh, K., & Fathi, M. (2018). Preparation and characterization of curcumin loaded gold/graphene oxide nanocomposite for potential breast cancer therapy. Research on Chemical Intermediates, 44, 7891-7904. https://doi.org/10.1007/s11164-018-3593-8.
Richardson, J. J., Cui, J., Bjornmalm, M., Braunger, J. A., Ejima, H., & Caruso, F. (2016). Innovation in layer-by-layer assembly. Chemical Reviews, 116(23), 14828-14867. https://doi.org/10.1021/acs.chemrev.6b00627.
Roudashti, S., Zeighami, H., Mirshahabi, H., Bahari, S., Soltani, A., & Haghi, F. (2017). Synergistic activity of sub-inhibitory concentrations of curcumin with ceftazidime and ciprofloxacin against Pseudomonas aeruginosa quorum sensing related genes and virulence traits. World Journal of Microbiology and Biotechnology, 33, 1-8. https://doi.org/10.1007/s11274-016-2195-0.
Sun, X., Liu, Z., Welsher, K., Robinson, J. T., Goodwin, A., Zaric, S., & Dai, H. (2008). Nano-graphene oxide for cellular imaging and drug delivery. Nano Research, 1, 203-212. https://doi.org/10.1007/s12274-008-8021-8.
Surdjawidjaja, J. E. (2012). Antagonism of vitamin C and vitamin E on action of quinolones. Universa Medicina, 31(2), 71-72. https://doi.org/10.18051/UnivMed.2012.v31.71-72.
Teow, S. Y., & Ali, S. A. (2015). Synergistic antibacterial activity of Curcumin with antibiotics against Staphylococcus aureus. Pakistan Journal of Pharmaceutical Sciences, 28(6), 2109-2114. https://doi.org/10.21203/rs.3.rs-1551439/v1.
Wang, F., Yuan, J., Zhang, Q., Yang, S., Jiang, S., & Huang, C. (2018). PTX-loaded three-layer PLGA/CS/ALG nanoparticle based on layer-by-layer method for cancer therapy. Journal of Biomaterials Science, 29(13), 1566-1578. https://doi.org/10.1080/09205063. 2018.1475941.
Wong, J. K., Mohseni, R., Hamidieh, A. A., MacLaren, R. E., Habib, N., & Seifalian, A. M. (2017). Limitations in clinical translation of nanoparticle-based gene therapy. Trends in Biotechnology, 35(12), 1124-1125. https://doi.org/10.1016/j.tibtech.2017.07.009.
Yadav, A., Lomash, V., Samim, M., & Flora, S. J. (2012). Curcumin encapsulated in chitosan nanoparticles: a novel strategy for the treatment of arsenic toxicity. Chemico-Biological Interactions, 199(1), 49-61. https://doi.org/10.1016/j.cbi.2012.05.011.
Yun, D. G., & Lee, D. G. (2016). Antibacterial activity of curcumin via apoptosis-like response in Escherichia coli. Applied Microbiology and Biotechnology, 100, 5505-5514. https://doi.org/10.1007/s00253-016-7415-x.
Zaaba, N. I., Foo, K. L., Hashim, U., Tan, S. J., Liu, W. W., & Voon, C. H. (2017). Synthesis of graphene oxide using modified hummers method: solvent influence. Procedia Engineering, 184, 469-477. https://doi.org/10.1016/j.proeng.2017.04.118.
Zhang, X., Yin, J., Peng, C., Hu, W., Zhu, Z., Li, W., ... & Huang, Q. (2011). Distribution and biocompatibility studies of graphene oxide in mice after intravenous administration. Carbon, 49(3), 986-995. https://doi.org/10.1016/j.carbon.2010.11.005.
Zheng, D., Huang, C., Huang, H., Zhao, Y., Khan, M. R. U., Zhao, H., & Huang, L. (2020). Antibacterial mechanism of curcumin: a review. Chemistry & Biodiversity, 17(8), e2000171. https://doi.org/10.1002/cbdv.202000171.
Zhu, Y., Murali, S., Cai, W., Li, X., Suk, J. W., Potts, J. R., & Ruoff, R. S. (2010). Graphene and graphene oxide: synthesis, properties, and applications. Advanced Materials, 22(35), 3906-3924. https://doi.org/10.1002/adma. 201001068.
Zokaei, E., Badoei-Dalfrad, A., Ansari, M., Karami, Z., Eslaminejad, T., & Nematollahi-Mahani, S. N. (2019). Therapeutic potential of DNAzyme loaded on chitosan/cyclodextrin nanoparticle to recovery of chemosensitivity in the MCF-7 cell line. Applied Biochemistry and Biotechnology, 187, 708-723. https://doi.org/10.1007/s12010-018-2836-x.