Polyphenols of four medicinal plants extracts and relation with antifungal activities through in vitro and in silico studies
DOI:
https://doi.org/10.5902/2179460X76669Keywords:
Medicinal plants, Polyphenols, HPLC-DAD, Molecular Docking, Candida albicansAbstract
Several medicinal plant´s extracts contain phenolic compounds with antifungal properties useful in pharmaceutical formulations. This study selected species from Cocó River State Park in Fortaleza, Ceará, Brazil, and compare their efficiency as antifungal products. To achieve this goal phenolic profile and anticandidal actions of extracts were evaluated, main constituents were characterized and correlated with antifungal properties through in vitro and in silico studies. Anacardium occidentale, Myracrodruon urundeuva, Laguncularia racemosa, and Terminalia catappa were chosen. The plant parts were collected in accordance with folk medicine recommendation. The main compounds present in the extracts were gallic acid, epicatechin, ellagic acid, isoquercitrin, quercetin and rutin, detected by high performance liquid chromatography analysis. The anticandidal activity of extracts varied from high to moderate, and A. occidentale present the best activity followed by L. racemosa. The in silico studies revealed that affinity energy (∆G) for ellagic acid (-9.4), isoquercitrin (-9.3) and rutin (-9.0) kcal moL-1 were better in relation to secreted aspartic proteinase 5 (Sap5) from Candida albicans, nevertheless ellagic acid and isoquercitrin act in different places in relation to the active site of Sap5 and could act in synergism with fluconazole.
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Ahad, A., Ganai, A.A., Mujeeb, M., & Siddiqui, W.A. (2014). Ellagic acid, an NF-κB inhibitor, ameliorates renal function in experimental diabetic nephropathy. Chem Biol Interact. 219, 64–75. https://doi.org/10.1016/j.cbi.2014.05.011 DOI: https://doi.org/10.1016/j.cbi.2014.05.011
Al Aboody, M.S., & Mickymaray, S. (2020). Anti-fungal efficacy and mechanisms of flavonoids. Antibiotics. 9, 45. https://doi.org/10.3390/antibiotics9020045 DOI: https://doi.org/10.3390/antibiotics9020045
Álvarez-Cilleros, D., Martín, M.Á., & Goya, L., Ramos, S. (2018) (-) -Epicatechin and the colonic metabolite 3,4-dihydroxyphenylacetic acid protect renal proximal tubular cell against high glucose-induced oxidative stress by modulating NOX-4/SIRT-1 signalling. J Funct Foods. 46, 19–28. https://doi.org/10.1016/j.jff.2018.04.051 DOI: https://doi.org/10.1016/j.jff.2018.04.051
Andrade Júnior, F.P., Alves, T.W.B., Romano, T.K.F., & Medeiros, F.D. (2018). Potencial antibacteriano e antifúngico de extratos de Anacardium occidentale. Per Tchê Quim. 15, 313-32. DOI: https://doi.org/10.52571/PTQ.v15.n30.2018.316_Periodico30_pgs_313_321.pdf
Apache, Autodocktools, version 1.5.7 rc1, The Scripps Research Institute, La Jolla, USA, 2007.
Araújo, J.M.D., Silva, A.P., Cândido, M.B., Silva, T.W.M., & Andrade Júnior, F.P. (2020). Ethnopharmacological Study of Anacardium occidentale: A Brief Review. Res., Soc. Dev. 9, E487985802. https://doi.org/10.33448/Rsd-V9i8.5802 DOI: https://doi.org/10.33448/rsd-v9i8.5802
Badhani, B., Sharma, N., & Kakkar, R. (2015). Gallic acid: A versatile antioxidant with promising therapeutic and industrial applications. RSC Advances. 5, 27540–27557. https://doi.org/10.1039/C5RA01911G DOI: https://doi.org/10.1039/C5RA01911G
Borelli, C., Ruge, E., Lee, J.H., Schaller, M., Vogelsang, A., Monod, M., Korting, H.C., Huber, R., & Maskos, K. (2008). X-ray structures of Sap1 and Sap5: Structural comparison of the secreted aspartic proteinases from Candida albicans. Proteins: Structure, Function, and Bioinformatics. 72, 1308–1319. https://doi.org/10.1002/prot.22021 DOI: https://doi.org/10.1002/prot.22021
ChemAxon. (2019). Marvin A full featured chemical editor for making science accessible on all platforms. https://chemaxon.com/products/marvin
Chobot, V., & Hadacek, F. (2011). Exploration of pro-oxidant and antioxidant activities of the flavonoid myricetin. Redox Report. 16, 242–247. https://doi.org/10.1179/1351000211Y.0000000015 DOI: https://doi.org/10.1179/1351000211Y.0000000015
Clinical and Laboratory Standards Institute (CLSI). (2018). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi (Approved Standard Document M38. CLSI). Clinical and Laboratory Standards Institute (CLSI). (2a ed.). Wayne, PA.
Csizmadia, P. (1999). Marvinsketch and marvinview: Molecule applets for the world wide web. Proceedings of the 3rd International Electronic Conference on Synthetic Organic Chemistry, 1775. https://doi.org/10.3390/ecsoc-3-01775 DOI: https://doi.org/10.3390/ecsoc-3-01775
Dastmalchi, S., Hamzeh-Mivehroud, M., & Sokouti, B. (Orgs.). (2016). Methods and algorithms for molecular docking-based drug design and discovery. Medical Information Science Reference, an imprint of IGI Global. DOI: https://doi.org/10.4018/978-1-5225-0115-2
Dimcheva, V., Kaloyanov, N., Karsheva, M., Peycheva, M.F., & Stoilova, N. (2019). HPLC-DAD method for simultaneous determination of natural polyphenols. Open J Anal Bioanal Chem. 3, 39-43. http://dx.doi.org/10.17352/ojabc.000009 DOI: https://doi.org/10.17352/ojabc.000009
Ekambaram, S.P., Perumal, S.S., & Balakrishnan, A. (2016). Scope of Hydrolysable Tannins as Possible Antimicrobial Agent. Phytother Res. 30, 1035-1045. https://doi.org/10.1002/ptr.5616 DOI: https://doi.org/10.1002/ptr.5616
Fontenelle, R.O.S., Morais, S.M., Brito, E.H.S., Kerntopf, M.R., Brilhante, R.S.N., Cordeiro, R.A., Tomé, A.R., Queiroz, M.G.R., Nascimento, N.R.F., Sidrim, J.J.C., & Rocha, M.F.G. (2007). Chemical composition, toxicological aspects and antifungal activity of essential oil from Lippia sidoides Cham. J Antimicrob Chemother. 59, 934–940. https://doi.org/10.1093/jac/dkm066 DOI: https://doi.org/10.1093/jac/dkm066
Frota, L., Alves, D., Freitas, L., Lopes, F., Marinho, M., Marinho, E., & Morais, S.(2022). In vitro antioxidant and anticholinesterase activities of Ouratea fieldingiana (Gardner) Eng. leaf extract and correlation with its phenolics profile with an in silico study in relation to Alzheimer’s disease. J Braz Chem Soc. https://doi.org/10.21577/0103-5053.20210163 DOI: https://doi.org/10.21577/0103-5053.20210163
Hai, Y., Zhang, Y., Liang, Y., Ma, X., Qi, X., Xiao, J., Xue, W., Luo, Y., & Yue, T. (2022). Advance on the absorption, metabolism, and efficacy exertion of quercetin and its important derivatives: Absorption, metabolism and function of quercetin. Food Frontiers. 1, 420–434. https://doi.org/10.1002/fft2.50 DOI: https://doi.org/10.1002/fft2.50
Hanwell, M.D., Curtis, D.E., Lonie, D.C., Vandermeersch, T., Zurek, E., & Hutchison, G.R. (2012). Avogadro: An advanced semantic chemical editor, visualization, and analysis platform. J Cheminformatics. 4, 17. https://doi.org/10.1186/1758-2946-4-17 DOI: https://doi.org/10.1186/1758-2946-4-17
Hasumura, M., Yasuhara, K., Tamura, T., Imai, T., Mitsumori, K., & Hirose, M. (2004). Evaluation of the toxicity of enzymatically decomposed rutin with 13-weeks dietary administration to Wistar rats. Food Chem Toxicol. 42, 439–444. https://doi.org/10.1016/j.fct.2003.10.006 DOI: https://doi.org/10.1016/j.fct.2003.10.006
Imberty, A., Hardman, K.D., Carver, J.P., & Perez, S. (1991). Molecular modelling of protein-carbohydrate interactions. Docking of monosaccharides in the binding site of concanavalin A. Glycobiology. 1, 631–642. https://doi.org/10.1093/glycob/1.6.631 DOI: https://doi.org/10.1093/glycob/1.6.631
Ivanov, M., Kannan, A., Stojković, D.S., Glamočlija, J., Calhelha, R.C., Ferreira, I.C.F.R., Sanglard, D., & Soković, M. (2020). Flavones, flavonols, and glycosylated derivatives - Impact on Candida albicans growth and virulence, expression of cdr1 and erg11, cytotoxicity. Pharmaceuticals. 14, 27. https://doi.org/10.3390/ph14010027 DOI: https://doi.org/10.3390/ph14010027
Janeczko, M., Gmur, D., Kochanowicz, E., Górka, K., & Skrzypek, T. (2022). Inhibitory effect of a combination of baicalein and quercetin flavonoids against Candida albicans strains isolated from the female reproductive system. Fungal Biology. https://doi.org/10.1016/j.funbio.2022.05.002 DOI: https://doi.org/10.1016/j.funbio.2022.05.002
Kadela-Tomanek, M., Jastrzębska, M., Marciniec, K., Chrobak, E., Bębenek, E., & Boryczka, S. (2021). Lipophilicity, pharmacokinetic properties, and molecular docking study on sars-cov-2 target for betulin triazole derivatives with attached 1,4-quinone. Pharmaceutics. 13, 781. https://doi.org/10.3390/pharmaceutics13060781 DOI: https://doi.org/10.3390/pharmaceutics13060781
Kessler, M., Ubeaud, G., & Jung, L. (2010). Anti- and pro-oxidant activity of rutin and quercetin derivatives. J Pharm Pharmacol. 55, 131–142. https://doi.org/10.1211/002235702559 DOI: https://doi.org/10.1211/002235702559
Kim, S., Woo, E.-R., & Lee, D.G. (2019). Synergistic antifungal activity of isoquercitrin: Apoptosis and membrane permeabilization related to reactive oxygen species in Candida albicans: synergy of iso is regulated by oxidative stress. IUBMB Life. 71, 283–292. https://doi.org/10.1002/iub.1973 DOI: https://doi.org/10.1002/iub.1973
Kumar, A., Kaushik, P., Incerpi, S., Pedersen, J.Z., Goel, S., Prasad, A.K., Rohil, V., Parmar, V.S., Saso, L., & Len, C. (2021). Evaluation of the free radical scavenging activities of ellagic acid and ellagic acid peracetate by epr spectrometry. Molecules. 26, 4800. https://doi.org/10.3390/molecules26164800 DOI: https://doi.org/10.3390/molecules26164800
Li, Z.-J., Liu, M., Dawuti, G., Dou, Q., Ma, Y., Liu, H.G., & Aibai, S. (2017). Antifungal activity of gallic acid in vitro and in vivo: Gallic acid, Candida albicans, ergosterol, cyp51, mice. Phytother Res. 31, 1039–1045. https://doi.org/10.1002/ptr.5823 DOI: https://doi.org/10.1002/ptr.5823
Lima Neto, G.A., Kaffashi, S., Luiz, W.T., Ferreira, W.R., Silva, Y.S.A.D., Pazin, G.V., & Violante, I.M.P. (2015). Quantificação de metabólitos secundários e avaliação da atividade antimicrobiana e antioxidante de algumas plantas selecionadas do Cerrado de Mato Grosso. Rev Bras Pl Med. 17, 1069–1077. https://doi.org/10.1590/1983-084x/14_161 DOI: https://doi.org/10.1590/1983-084x/14_161
Maeta, K., Nomura, W., Takatsume, Y., Izawa, S., & Inoue, Y. (2007). Green tea polyphenols function as prooxidants to activate oxidative-stress-responsive transcription factors in yeasts. Appl Environ Microbiol. 73, 572–580. https://doi.org/10.1128/AEM.01963-06 DOI: https://doi.org/10.1128/AEM.01963-06
Miranda-Buendia, E., González-Gómez, G.H., Falcón-Neri, M.A., Durán-Pastén, M.L., Jiménez-Martínez, C., Vera-Graziano, R., Ospina-Orejarena, A., Rivera-Torres, F., Prado-Villegas, G., & Maciel-Cerda, A. (2022). Activity patterns of cardiomyocytes in electrospun scaffolds of poly (Ε-caprolactone), collagen, and epicatechin. Mater Today Commun. 31, 103405. https://doi.org/10.1016/j.mtcomm.2022.103405 DOI: https://doi.org/10.1016/j.mtcomm.2022.103405
Morais, S. M., Lopes, F.F.S., Fontenele, G.A., Silva, M.V.F., Fernandes, V.B., & Alves, D.R. (2021). Total phenolic content and antioxidant and anticholinesterase activities of medicinal plants from the State’s Cocó Park (Fortaleza-ce, Brazil). Res., Soc. Dev. 10, e7510514493. https://doi.org/10.33448/rsd-v10i5.1449 DOI: https://doi.org/10.33448/rsd-v10i5.14493
Neves, A.M., Morais, S.M., Santos, H.S., Ferreira, M.M., Cruz, R.C.V., Souza, E.B., Andrade, L.B.S., & Fontenelle, R.O.S. (2022). Prospecção química, atividade antioxidante, anticolinesterásica e antifúngica de extratos etanólicos de espécies de Senna Mill. (Fabaceae). Hoehnea. 49. https://doi.org/10.1590/2236-8906-111/2020. DOI: https://doi.org/10.1590/2236-8906-111/2020
Oliveira, F.A.D., Rorato, V.C., Almeida-Apolonio, A.A., Rodrigues, A.B., Barros, A.L.D., Sangalli, A., Arena, A.C., Mota, J.S., Grisolia, A.B., & Oliveira, K.M.P.D. (2017). In vitro antifungal activity of Myracrodruon urundeuva Allemão against human vaginal Candida species. An. Acad. Bras. Ciênc. 89, 2423-2432. https://doi.org/10.1590/0001-3765201720170254. DOI: https://doi.org/10.1590/0001-3765201720170254
Panche, A.N., Diwan, A.D., & Chandra, S.R. (2016). Flavonoids: An overview. J Nutr Sci. 5, e47. https://doi.org/10.1017/jns.2016.41 DOI: https://doi.org/10.1017/jns.2016.41
Rossatto, F.C.P., Tharmalingam, N., Escobar, I.E., D’Azevedo, P.A., Zimmer, K.R., & Mylonakis, E. (2021). Antifungal activity of the phenolic compounds Ellagic acid (Ea) and Caffeic acid phenethyl ester (Cape) against drug-resistant Candida auris. J Fungi. 7, 763. https://doi.org/10.3390/jof7090763 DOI: https://doi.org/10.3390/jof7090763
Sartoratto, A., Machado, A.L.M., Delamerlina, C., Figueira, G.M., Duarte, M.C.T., & Rehder, V.L.G. (2004). Composition and antimicrobial activity of essential oils from aromatic plants used in Brazil. Braz J Microbiol. 35, 275-280. https://doi.org/10.1590/S1517-83822004000300001 DOI: https://doi.org/10.1590/S1517-83822004000300001
Seleem, D., Pardia, V., & Murata, R.M. (2017). Review of flavonoids: A diverse group of natural compounds with anti-Candida albicans activity in vitro. Arch Oral Biol. 76, 76-83. https://doi.org/10.1016/j.archoralbio.2016.08.030 DOI: https://doi.org/10.1016/j.archoralbio.2016.08.030
Semwal, R., Joshi, S.K., Semwal, R.B., & Semwal, D.K. (2021). Health benefits and limitations of rutin - A natural flavonoid with high nutraceutical value. Phytochem Lett. 46, 119–128, 2021. https://doi.org/10.1016/j.phytol.2021.10.006 DOI: https://doi.org/10.1016/j.phytol.2021.10.006
Shityakov, S., & Foerster, C. (2014). In silico predictive model to determine vector-mediated transport properties for the blood-brain barrier choline transporter. Adv Appl Bioinform Chem. 23. https://doi.org/10.2147/AABC.S63749 DOI: https://doi.org/10.2147/AABC.S63749
Silva, L.J., Silva, C.R., Sá, L.G., Barroso, F.D., Cândido, T.M., Queiroz, H.A., Moreira, L.E.A., Baccallini, O.V., Cavalcanti, B.C., Silva, J., Marinho, E.S., Moraes, M.O., Neto, J.B., & Júnior, H.V. (2022). Antifungal activity of dexamethasone against fluconazole-resistant Candida albicans and its activity against biofilms. Future Microbiol. 17, 607–620. https://doi.org/10.2217/fmb-2021-0146. DOI: https://doi.org/10.2217/fmb-2021-0146
Silva, N.F., Silva, E.R.A., Silva, G.N.B., Silva, M.E.B., Espindola, M.T.A., Correia, S.D.O.S., Falcão, R.E.A., & Castanha, E.R. (2021). Ethnopharmacological study and antifungal properties of two medicinal species: Anacardium occidentale (Linn) (Cajueiro, Anacardiaceae) and Schinus terebinthifolius Raddi (Aroeira, Anacardiaceae). Braz J Dev. 7, 9791–9806. https://doi.org/10.34117/bjdv7n1-664. DOI: https://doi.org/10.34117/bjdv7n1-664
Silva, M.A., Almeida, A.C., Arruda, F.V.F., & Gusmão, N. B. (2011). Endophytic fungi from Brazilian mangrove plant Laguncularia racemosa (L.) Gaertn. (Combretaceae): their antimicrobial potential. Sci Microbial Path: Comm Curr Res Technol Adv. 2.
Spampinato, C., & Leonardi, D. (2013) Candida infections, causes, targets, and resistance mechanisms: Traditional and alternative antifungal agents. BioMed Research International. 1–13. https://doi.org/10.1155/2013/204237 DOI: https://doi.org/10.1155/2013/204237
Sun, Y., Li, C., Li, Z., Shangguan, A., Jiang, J., Zeng, W., Zhang, S., & He, Q. (2021). Quercetin as an antiviral agent inhibits the Pseudorabies virus in vitro and in vivo. Virus Research. 305, 198556. https://doi.org/10.1016/j.virusres.2021.198556 DOI: https://doi.org/10.1016/j.virusres.2021.198556
Teodoro, G. R., Ellepola, K., Seneviratne, C. J., & Koga-Ito, C. Y. (2015). Potential use of phenolic acids as anti-candida agents: A review. Front Microbiol. 6, 1420. https://doi.org/10.3389/fmicb.2015.01420 DOI: https://doi.org/10.3389/fmicb.2015.01420
Terças, A.G., Monteiro, A.S., Moffa, E.B., Santos, J.R.A., Sousa, E.M., Pinto, A.R.B., Costa, P.C.S., Borges, A.C.R., Torres, L.M.B., Barros Filho, A.K. D., Fernandes, E.S., & Monteiro, C.A. (2017). Phytochemical characterization of Terminalia catappa Linn. extracts and their antifungal activities against Candida spp. Front. Microbiol. 8, 595. https://doi.org/10.3389/fmicb.2017.00595 DOI: https://doi.org/10.3389/fmicb.2017.00595
Valentová, K.., Vrba, J., Bancířová, M., Ulrichová, J., & Křen, V. (2014). Isoquercitrin: Pharmacology, toxicology, and metabolism. Food Chem Toxicol. 68, 267–282. https://doi.org/10.1016/j.fct.2014.03.018 DOI: https://doi.org/10.1016/j.fct.2014.03.018
Viana, A.R., Noro, B.G., Santos, D., Wolf, K., Neves, Y.S., Moresco, R.N., Ourique, A.F., Flores, E.M.M., Rhoden, C.R.B., & Krause, L.M.F. (2022). Detection of new phytochemical compounds from Vassobia breviflora (Sendtn.) Hunz: antioxidant, cytotoxic, and antibacterial activity of the hexane extract. J Toxicol Environ Health, 86, 51-68. http://dx.doi.org/10.1080/15287394.2022.2156956 DOI: https://doi.org/10.1080/15287394.2022.2156956
Wang, J., Zhang, C., Zhang, J., Xie, J., Yang, L., Xing, Y., & Li, Z. (2020). The effects of quercetin on immunity, antioxidant indices, and disease resistance in zebrafish (Danio rerio). Fish Physiol Biochem. 46, 759–770. https://doi.org/10.1007/s10695-019-00750-2 DOI: https://doi.org/10.1007/s10695-019-00750-2
Yan, J., Zhang, G., Pan, J., & Wang, Y. (2014). α-Glucosidase inhibition by luteolin: Kinetics, interaction and molecular docking. Int J Biol Macromol. 64, 213–223. https://doi.org/10.1016/j.ijbiomac.2013.12.007 DOI: https://doi.org/10.1016/j.ijbiomac.2013.12.007
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