Phenolic profile and antioxidant, anticholinesterase and anti- candida potential evaluation in vitro and in silico studies of Tapirira guianensis Aubl. extracts
DOI:
https://doi.org/10.33448/rsd-v11i13.35378Keywords:
Tapirira guianensis; Antioxidant; Acetilcolinesterase; Anti-Candida.Abstract
Polar extracts of Tapirira guianensis Aubl. were prepared for evaluation of biological activities. Identification and quantification of phenolic compounds, antioxidant activity, inhibition of acetylcholinesterase enzyme and antifungal potential were performed in all extracts. High contents of total phenols were detected in the ethanolic and aqueous extracts of the leaves (237.10±5.39 mg EAG/g and 346.46±5.67 mg EAG) respectively. The same extracts had a free radical scavenging potential by both DPPH and ABTS+ methods. Ethanolic extract of the leaves with IC50= 15.06±0.02 µg/mL and 16.49±0.01µg/mL) and aqueous extracts (11.54±0.01 µg/mL and 15.14±0.02 µg/mL respectively. In the study by high-performance liquid chromatography the phenolic substances were recorded: gallic acid, rutin, ellagic acid, quercetin and apigenin in the leaves and gallic acid and quercetin in the stem bark. Ethanolic and aqueous extracts of the leaves and stem bark showed high potency of inhibiting the enzyme acetylcholinesterase, with IC50 values = 13.94±0.02 µg/mL, 13.69±0.08 µg/mL and 14.79±0.20 µg/mL respectively. The aqueous extract of the leaves showed anti-Candida action against all four strains of the microorganism. The in silico studies evidenced that all the ligands analyzed presented interaction with the SAP5 protein highlighting the ellagic acid, the rutin and the quercetin. With these results, the activities previously reported for the species T. guianensis are confirmed, highlighting the polar extracts, mainly aqueous as a source of antioxidant, acetylcholinesterase inhibitor and antifungal substances.
References
Ademosun, A. O., Oboh, G., Bello, F., & Ayeni, P. O. (2016). Antioxidative Properties and Effect of Quercetin and Its Glycosylated Form (Rutin) on Acetylcholinesterase and Butyrylcholinesterase Activities. Journal of evidence-based complementary & alternative medicine, 21(4), 11-17. https://doi.org/10.1177/2156587215610032
Antonopoulou, I., Sapountzaki, E., Rova, U., & Christakopoulos, P. (2022). The Inhibitory Potential of Ferulic Acid Derivatives against the SARS-CoV-2 Main Protease: Molecular Docking, Molecular Dynamics, and ADMET Evaluation. Biomedicines, 10(8), 1787. https://doi.org/10.3390/biomedicines10081787
Araújo, C. R. M., Santos, V. L. dos A., & Arlan, A. G. (2016). Acetilcolinesterase - AChE: Uma Enzima de Interesse Farmacológico. Revista Virtual de Química, 8(6), 1818–1834
Badhani, B., Sharma, N., & Kakkar, R. (2015). Ácido gálico: um antioxidante versátil com aplicações terapêuticas e industriais promissoras. Rsc Advances, 5 (35), 27540-27557. https://doi.org/10.1039/C5RA01911G
Barbosa, F. G., Lima, M. A. S.., Braz-Filho, R., & Silveira, E R. (2006). Glicosídeos iridóides e feniletanoides de Lippia alba. Biochemical Systematics and Ecology, 11 (34), 819-821. https://doi.org/10.1016/j.bse.2006.06.006
Becker, M., Nunes, G., Ribeiro, D., Silva, F., Catanante, G., & Marty, J. (2019). Determination of the Antioxidant Capacity of Red Fruits by Miniaturized Spectrophotometry Assays. Journal of the Brazilian Chemical Society, 3(4), 223–227. https://doi.org/10.21577/0103-5053.20190003
Biovia, D. S., Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., & Richmond, T. J. (2000). Dassault Systèmes BIOVIA, Discovery Studio Visualizer. The Journal of Chemical Physics, 17(2).
Borelli, C., Ruge, E., Lee, J. H., Schaller, M., Vogelsang, A., Monod, M., & 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(4), 1308-1319. https://doi.org/10.1002/prot.22021
Bors, W., & Saran, M. (1987). Radical scavenging by flavonoid antioxidants. Free radical research communications, 2(4-6), 289-294. https://doi.org/10.3109/10715768709065294
Clinical and Laboratory Standards Institute (CLSI, formerly National Commitee for Clinical and Laboratory Standards NCCLS) (2018). Method M-38ª, (2ª ed), Wayne, Ed.; NCCLS Pennsylvania, 22 (16) 1-27
Correia, S. D. J., DavidI, J. M., Silva, E. P. D., David, J. P., Lopes, L. M., & Guedes, M. L. S. (2008). Flavonóides, norisoprenóides e outros terpenos das folhas de Tapirira guianensis . Química Nova, 31, 2056-2059. https://doi.org/10.1590/S0100-40422008000800027
Csizmadia, P. (1999) In Proceedings of The 3rd International Electronic Conference on Synthetic Organic Chemistry; MDPI: Basel, Switzerland, 1775.
da Silva, C. R., Moura, F. L. D., Alves Filho, A. L. A., de Sousa Campos, R., de Farias Cabral, V. P., Sá, L. G. D. A. V., & Neto, J. B. D. A. (2022). Evaluation of interactions of silibinin with the proteins ALS3 and SAP5 against Candida albicans. Journal of Health & Biological Sciences, 10(1), 1-6. http://dx.doi.org/10.12662/2317-3076jhbs.v10i1.4239.p1-6.2022
da Silva, L. J., Barroso, F. D. D., Vieira, L. S., Mota, D. R. C., da Silva Firmino, B. K., da Silva, C. R., & de Andrade Neto, J. B. (2021). Diazepam’s antifungal activity in fluconazole-resistant Candida spp. and biofilm inhibition in C. albicans: evaluation of the relationship with the proteins ALS3 and SAP5. Journal of Medical Microbiology, 70(3), 001308. https://doi.org/10.1099/jmm.0.001308
D'Andrea, G. (2015). Quercetin: a flavonol with multifaceted therapeutic applications?. Fitoterapia, 106, 256-271. https://doi.org/10.1016/j.fitote.2015.09.018
David, J. M., Chávez, J. P., Chai, H. B., Pezzuto, J. M., & Cordell, G. A. (1998). Two new cytotoxic compounds from Tapirira guianensis . Journal of natural products, 61(2), 287-289. https://doi.org/10.1021/np970422v
de Andrade Neto, J. B., de Farias Cabral, V. P., Nogueira, L. F. B., da Silva, C. R., Sa, L. G. D. A. V., da Silva, A. R., & Júnior, H. V. N. (2021). Anti-MRSA activity of curcumin in planktonic cells and biofilms and determination of possible action mechanisms. Microbial pathogenesis, 155, 104892. https://doi.org/10.1016/j.micpath.2021.104892
de Morais, S. M., da Silva Lopes, F. F., Fontenele, G. A., da 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). Research, Society and Development, 10(5), e7510514493-e7510514493. https://doi.org/10.33448/rsd-v10i5.14493
Duthie, G. G., Duthie, S. J., & Kyle, J. A. (2000). Plant polyphenols in cancer and heart disease: implications as nutritional antioxidants. Nutrition research reviews, 13(1), 79-106. https://doi.org/10.1079/095442200108729016
Ekambaram, S. P., Perumal, S. S., & Balakrishnan, A.(2016). Phytotherapy research 30, 1035. https://doi.org/10.1002/ptr.5616
Ellman, G. L., Courtney, K. D., Andres, V., & Featherstone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology, 7(2), 88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Fontenelle, R. O. S., Morais, S. M., Brito, E. H. S., Kerntopf, M. R., Brilhante, R. S. N., Cordeiro, R. A., & Rocha, M. F. G. (2007). Chemical composition, toxicological aspects and antifungal activity of essential oil from Lippia sidoides Cham. Journal of Antimicrobial Chemotherapy, 59(5), 934-940. https://doi.org/10.1093/jac/dkm066
Frota, L. S., Lopes, F. F. S., Alves, D. R., Freitas, L. S., Franco, G. M. G., & Morais, S. M. de. (2021). Composição química e avaliação das atividades antioxidante e anticolinesterásica do óleo dos frutos de Ouratea fieldingiana (Gargner) Engl. Research, Society and Development, 10(10), e532101019013. https://doi.org/10.33448/rsd-v10i10.19013
Funari, C. S., & Ferro, V. O. (2006). Análise de própolis. Food Science and Technology, 26, 171-178. https://doi.org/10.1590/S0101-20612006000100028
Gupta, A., Kumar, R., Ganguly, R., Singh, A. K., Rana, H. K., & Pandey, A. K. (2021). Antioxidant, anti-inflammatory and hepatoprotective activities of Terminalia bellirica and its bioactive component ellagic acid against diclofenac induced oxidative stress and hepatotoxicity. Toxicology reports, 8, 44-52. https://doi.org/10.1016/j.toxrep.2020.12.010
Halgren, T. A. (1996). Merck molecular force field. II. MMFF94 van der Waals and electrostatic parameters for intermolecular interactions. Journal of Computational Chemistry, 17(5–6), 520–552. https://doi.org/10.1002/(SICI)1096-987X(199604)17:5/6<520::AID-JCC2>3.0.CO;2-W
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. Journal of Cheminformatics, 4(1), 17. https://doi.org/10.1186/1758-2946-4-17
Huey, R., Morris, G. M., & Forli, S. (2012). Using AutoDock 4 and AutoDock vina with AutoDockTools: a tutorial. The Scripps Research Institute Molecular Graphics Laboratory, 10550, 92037.
Imani, A., Maleki, N., Bohlouli, S., Kouhsoltani, M., Sharifi, S., & Maleki Dizaj, S. (2021). Molecular mechanisms of anticancer effect of rutin. Phytotherapy Research, 35(5), 2500-2513. https://doi.org/10.1002/ptr.6977
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(6), 631-642. https://doi.org/10.1093/glycob/1.6.631
Ivanov, M., Kannan, A., Stojković, D. S., Glamočlija, J., Calhelha, R. C., Ferreira, I. C., & Soković, M. (2020). Flavones, flavonols, and glycosylated derivatives impact on Candida albicans growth and virulence, expression of cdr1 and erg11, cytotoxicity. Pharmaceuticals, 14(1), 27. 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, 126(6-7), 407-420. https://doi.org/10.1016/j.funbio.2022.05.002
Kim, G. H., Kim, J. E., Rhie, S. J., & Yoon, S. (2015). The role of oxidative stress in neurodegenerative diseases. Experimental neurobiology, 24(4), 325.
Kwun, M. S., & Lee, D. G. (2020). Quercetin-induced yeast apoptosis through mitochondrial dysfunction under the accumulation of magnesium in Candida albicans. Fungal biology, 124(2), 83-90. https://doi.org/10.1016/j.funbio.2019.11.009
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. Phytotherapy research, 31(7), 1039-1045. https://doi.org/10.1002/ptr.5823
Marinho, E. M., de Andrade Neto, J. B., Silva, J., da Silva, C. R., Cavalcanti, B. C., Marinho, E. S., & Júnior, H. V. N. (2020). Virtual screening based on molecular docking of possible inhibitors of Covid-19 main protease. Microbial Pathogenesis, 148, 104365. https://doi.org/10.1016/j.micpath.2020.104365
Meenambiga, S. S., Venkataraghavan, R., & Biswal, R. A. (2018). In silico analysis of plant phytochemicals against secreted aspartic proteinase enzyme of Candida albicans. Journal of Applied Pharmaceutical Science, 8(11), 140-150.
Naves, P. L. F., Santana, D. P., Ribeiro, E. L., & Menezes, A. C. S. (2013). Novas abordagens sobre os fatores de virulência de Candida albicans. Revista de Ciências Médicas e Biológicas, 12(2), 229-233. https://doi.org/10.9771/cmbio.v12i2.6953
Neves, A. M., Morais, S. M. D., Santos, H. S. D., Ferreira, M. M., Cruz, R. C. V., Souza, E. B. D., & Fontenelle, R. O. D. 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
Ngameni, B., Fotso, G. W., Kamga, J., Ambassa, P., Abdou, T., Fankam, A. G., & Kuete, V. (2013). Flavonoids and Related Compounds from the Medicinal Plants of Africa. In Medicinal Plant Research in Africa (pp. 301–350). Elsevier. https://doi.org/10.1016/B978-0-12-405927-6.00009-6
Ohno, Y., Fukuda, K., Takemura, G., Toyota, M., Watanabe, M., Yasuda, N., & Fujiwara, H. (1999). Induction of apoptosis by gallic acid in lung cancer cells. Anti-cancer drugs, 10(9), 845-851. https://doi.org/10.1097/00001813-199910000-00008
Patient, A., Jean-Marie, E., Robinson, J. C., Martial, K., Meudec, E., Levalois-Grützmacher, J., & Bereau, D. (2022). Polyphenol Composition and Antioxidant Activity of Tapirira guianensis Aubl.(Anarcadiaceae) Leaves. Plants, 11(3), 326. https://doi.org/10.3390/plants11030326
Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera - A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
Raina, K., Rajamanickam, S., Deep, G., Singh, M., Agarwal, R., & Agarwal, C. (2008). Chemopreventive effects of oral gallic acid feeding on tumor growth and progression in TRAMP mice. Molecular cancer therapeutics, 7(5), 1258-1267. https://doi.org/10.1158/1535-7163.MCT-07-2220
Rao, A. S., & Camilleri, M. (2010). metoclopramide and tardive dyskinesia. Alimentary pharmacology & therapeutics, 31(1), 11-19. https://doi.org/10.1111/j.1365-2036.2009.04189.x
Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., & Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free radical biology and medicine, 26(9-10), 1231-1237. https://doi.org/10.1016/S0891-5849(98)00315-3
Ren, L., Zhang, J., & Zhang, T. (2021). Immunomodulatory activities of polysaccharides from Ganoderma on immune effector cells. Food Chemistry, 340, 127933. https://doi.org/10.1016/j.foodchem.2020.127933
Rodrigues, A. M., Guimarães, D. O., Konno, T. U., Tinoco, L. W., Barth, T., Aguiar, F. A., & Muzitano, M. F. (2017). Phytochemical study of Tapirira guianensis leaves guided by vasodilatory and antioxidant activities. Molecules, 22(2), 304. https://doi.org/10.3390/molecules22020304
Roumy, V., Fabre, N., Portet, B., Bourdy, G., Acebey, L., Vigor, C., & Moulis, C. (2009). Four anti-protozoal and anti-bacterial compounds from Tapirira guianensis . Phytochemistry, 70(2), 305-311. https://doi.org/10.1016/j.phytochem.2008.10.003
Santos, T. C. D., Gomes, T. M., Pinto, B. A. S., Camara, A. L., & Paes, A. M. D. A. (2018). Naturally occurring acetylcholinesterase inhibitors and their potential use for Alzheimer's disease therapy. Frontiers in Pharmacology, 9, 1192. https://doi.org/10.3389/fphar.2018.01192
Schelenz, S. (2008). Management of candidiasis in the intensive care unit. Journal of Antimicrobial Chemotherapy, 61(suppl_1), i31-i34.
Schrödinger, L. L. C. The PyMOL Molecular Graphics System, Version 2.3. 2019. Google Scholar There is no corresponding record for this reference.
Seleem, D., Pardi, V., & Murata, R. M. (2017). Review of flavonoids: A diverse group of natural compounds with anti-Candida albicans activity in vitro. Archives of oral biology, 76, 76-83. https://doi.org/10.1016/j.archoralbio.2016.08.030
Sharma, A., Kashyap, D., Sak, K., Tuli, H. S., & Sharma, A. K. (2018). Therapeutic charm of quercetin and its derivatives: a review of research and patents. Pharmaceutical patent analyst, 7(1), 15-32. https://doi.org/10.4155/ppa-2017-0030
Shityakov, S., & Förster, C. (2014). In silico predictive model to determine vector-mediated transport properties for the blood–brain barrier choline transporter. Advances and applications in bioinformatics and chemistry: AABC, 7, 23. https://doi.org/10.2147/AABC.S63749
Silva, E. P. D., David, J. M., David, J. P., Garcia, G. H. T., & Silva, M. T. (2020). Chemical composition of biological active extracts of Tapirira guianensis (Anacardiaceae). Química Nova, 43, 1216-1219. https://doi.org/10.21577/0100-4042.20170605
Silva, J., Rocha, M. N., & Marinho, E. M. (2021). Evaluation of the ADME, toxicological analysis and molecular docking studies of the anacardic acid derivatives with potential antibacterial effects against staphylococcus aureus. J Anal Pharm Res, 10(5), 177-194. https://doi.org/10.15406/japlr.2021.10.00384
Silva-Oliveira, R. J., Lopes, G. F., Camargos, L. F., Ribeiro, A. M., Santos, F. V. D., Severino, R. P., & Ribeiro, R. I. M. D. A. (2016). Tapirira guianensis Aubl. extracts inhibit proliferation and migration of oral cancer cells lines. International journal of molecular sciences, 17(11), 1839. https://doi.org/10.3390/ijms17111839
Singh, D., Khan, M. A., Akhtar, K., Arjmand, F., & Siddique, H. R. (2022). Apigenin alleviates cancer drug Sorafenib induced multiple toxic effects in Swiss albino mice via anti-oxidative stress. Toxicology and Applied Pharmacology, 447, 116072. https://doi.org/10.1016/j.taap.2022.116072
Smiljkovic, M., Stanisavljevic, D., Stojkovic, D., Petrovic, I., Vicentic, J. M., Popovic, J., & Sokovic, M. (2017). Apigenin-7-O-glucoside versus apigenin: Insight into the modes of anticandidal and cytotoxic actions. EXCLI journal, 16, 795. https://doi.org/10.17179/excli2017-300
Sousa, C. M. D. M., Silva, H. R., Ayres, M. C. C., Costa, C. L. S. D., Araújo, D. S., Cavalcante, L. C. D., & Chaves, M. H. (2007). Fenóis totais e atividade antioxidante de cinco plantas medicinais. Química nova, 30, 351-355. https://doi.org/10.1590/S0100-40422007000200021
Trott, O., & Olson, A. J. (2009). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455–461. https://doi.org/10.1002/jcc.21334
Trubiano, J. A., & Padiglione, A. A. (2015). Nosocomial infections in the intensive care unit. Anaesthesia & Intensive Care Medicine, 16(12), 598-602.
Wang, W., Sun, C., Mao, L., Ma, P., Liu, F., Yang, J., & Gao, Y. (2016). The biological activities, chemical stability, metabolism and delivery systems of quercetin: A review. Trends in Food Science & Technology, 56, 21-38. https://doi.org/10.1016/j.tifs.2016.07.004
Yan, J., Zhang, G., Pan, J., & Wang, Y. (2014). α-Glucosidase inhibition by luteolin: Kinetics, interaction and molecular docking. International journal of biological macromolecules, 64, 213-223. https://doi.org/10.1016/j.ijbiomac.2013.12.007
Yan, X., Qi, M., Li, P., Zhan, Y., & Shao, H. (2017). Apigenin in cancer therapy: Anti-cancer effects and mechanisms of action. Cell & Bioscience, 7(1), 1-16. https://doi.org/10.1186/s13578-017-0179-x
Yang, J., Guo, J., & Yuan, J. (2008). In vitro antioxidant properties of rutin. LWT-Food Science and Technology, 41(6), 1060-1066. https://doi.org/10.1016/j.lwt.2007.06.010
Yusuf, D., Davis, A. M., Kleywegt, G. J., & Schmitt, S. (2008). An alternative method for the evaluation of docking performance: RSR vs RMSD. Journal of chemical information and modeling, 48(7), 1411-1422. https://doi.org/10.1021/ci800084x
Zhang, T., Zhong, S., Li, T., & Zhang, J. (2020). Saponins as modulators of nuclear receptors. Critical reviews in food science and nutrition, 60(1), 94-107. https://doi.org/10.1080/10408398.2018.1514580
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Copyright (c) 2022 Daniel Pereira de Oliveira; Selene Maia de Morais; Francisco Flávio da Silva Lopes; Daniela Ribeiro Alves; José Ribamar Garcez Neto; Raquel Oliveira dos Santos Fontenelle; Júlio Cesar Sousa Prado; Emmanuel da Silva Marinho; Márcia Machado Marinho; Lucas Lima Bezerra
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