Phenolic profile, antioxidant and antifungal activity of extracts from four medicinal plants of the Anacardiaceae family
DOI:
https://doi.org/10.33448/rsd-v10i8.17421Keywords:
Biological activities; Plant species; Cocó State Park; Free radicals.Abstract
El objetivo de este estudio fue evaluar el perfil químico y las actividades antioxidantes y antifúngicas de los extractos etanólicos de cuatro especies de Anacardiaceae, incluyendo también el estudio computacional del mecanismo de acción de los compuestos fenólicos contra la enzima espartato de Trichophyton rubrum semialdehído deshidrogenas aspartate. Para ello, se determinó el contenido de fenoles y flavonoides en los extractos. La actividad antifúngica de los extractos se evaluó mediante microdilución en caldo sobre hongos T. rubrum y la capacidad antioxidante se analizó midiendo el efecto eliminador de los extractos contra el radical 2,2'-difenil-1-picrilhidrazilo (DPPH). Para el estudio del acoplamiento molecular, se realizaron simulaciones por computadora de la interacción entre la enzima y los ligandos utilizando el AutoDock Vina Code. Los contenidos fenólicos y flavonoides variaron de 227,47 ± 18,62 a 493,44 ± 13,89 equivalente de ácido gálico (EAG), 14,86 ± 0,22 a 86,07 ± 1,67 equivalente de quercetina (EQ), respectivamente. La actividad antioxidante osciló entre 3,73 ± 0,12 y 11,21 ± 0,49 µg / ml, especialmente para Spondias mombim. Los extractos de etanol mostraron actividad antifúngica contra la mayoría de las cepas de T. rubrum. Los compuestos rutina, ácido elágico, quercetina, isoquercitrina y mangiferina, presentes en la especie, mostraran una mayor afinidad por la enzima aspartato semialdehído deshidrogenasa que el fluconazol, el antifúngico padron. Estos resultados proporcionan evidencia de que los extractos etanólicos de Anacardiaceae pueden ser fuentes potenciales de nuevos productos biotecnológicos, actuando como agentes antioxidantes y antifúngicos naturales.
References
Abdullah, A. H., Mohammed, A. S., & Abdullah, R. (2015). Identification and quantification of phenolic compounds in Mangifera indica waterlily kernel and their free radical scavenging activity. Journal of Advanced Agricultural Technologies, 2(1), 1-7. https://doi.org/10.12720/joaat.2.1.1-7.
Agedah, C. E., Bawo, D. D. S., & Nyananyo, B. L. (2010). Identification of antimicrobial properties of cashew, Anacardium occidentale L. (Family Anacardiaceae). Journal of Applied Science and Environmental Management, 14(3), 25-27. https://doi.org/ 10.4314/jasem.v14i3.61455.
Arya, R., Babu, V., & Ilyas, M. (1989). Phytochemical examination of the leaves of Anacardium-occidentale. Journal of the Indian Chemical Society, 66(1), 67-68.
Ajileye, O. O., Obuotor, E. M., Akinkunmi, E. O., & Aderogba, M. A. (2015). Isolation and characterization of antioxidant and antimicrobial compounds from Anacardium occidentale L. (Anacardiaceae) leaf extract. Journal of King Saud University-Science, 27(3), 244-252. https://doi.org/10.1016/j.jksus.2014.12.004.
Akroum, S. (2018). Antifungal activity of camellia sinensis crude extracts against four species of Candida and Microsporum persicolor. Journal de mycologie medicale, 28(3), 424-427. https://doi.org/10.1016/j.mycmed.2018.06.003.
Andrade, L. B. D. S., Julião, M. S. D. S., Cruz, R. C. V., Rodrigues, T. H. S., Fontenelle, R. O. D. S., & Silva, A. L. C. D. (2018). Antioxidant and antifungal activity of carnauba wax powder extracts. Industrial Crops and Products, 125(1), 220-227. https://doi.org/10.1016/j.indcrop.2018.09.004.
Araújo, A. A. D., Soares, L. A. L., Ferreira, M. R. A., Neto, M. A. D. S., Silva, G. R. D., Araújo Júnior, R. F. D., Guerra, G. C. B., & Melo, M. C. N. D. (2014). Quantification of polyphenols and evaluation of antimicrobial, analgesic and anti-inflammatory activities of aqueous and acetone–water extracts of Libidibia ferrea, Parapiptadenia rigida and Psidium guajava. Journal of ethnopharmacology, 156(28), 88-96. https://doi.org/10.1016/j.jep.2014.07.031.
Bardakci, H., Celep, E., Gözet, T., Kan, Y., & Kirmizibekmez, H. (2019). Phytochemical characterization and antioxidant activities of the fruit extracts of several Crataegus taxa. South African Journal of Botany, 124, 5-13. https://doi.org/10.1016/j.sajb.2019.04.012.
BIOVIA SDDS (2020) Discovery studio visualizer.
Bitencourt, T. A., Komoto, T. T., Massaroto, B. G., Miranda, C. E. S., Beleboni, R. O., Marins, M., & Fachin, A. L. (2013). Trans-chalcone and quercetin down-regulate fatty acid synthase gene expression and reduce ergosterol content in the human pathogenic dermatophyte Trichophyton rubrum. BMC complementary and alternative medicine, 13(1), 1-6. http://www.biomedcentral.com/1472-6882/13/229.
Cabral, B., Siqueira, E., Bitencourt., M. A., Lima, M. C., Lima, A. K., Ortmann, C. F., & Reginatto, F. H. (2016). Phytochemical study and anti-inflammatory and antioxidant potential of Spondias mombin leaves. Revista Brasileira de Farmacognosia, 26(3), 304-311. http://dx.doi.org/10.1016/j.bjp.2016.02.002.
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 th ed.). Wayne, PA.
Chotphruethipong, L., Benjakul, S., & Kijroongrojana, K. (2017). Optimization of extraction of antioxidative phenolic compounds from cashew (Anacardium occidentale L.) leaves using response surface methodology. Journal of Food Biochemistry, 41(4), 1-10. https://doi.org/10.1111/jfbc.12379.
Disegha, G. C., & Akani, N. P. (2017). Antifungal activity of Mangifera indica leaf extracts on selected fungi. Science and Technology, 4(2), 136-148. https://www.researchgate.net/profile/Nedie-Akani/publication/331574530.
Du, X., Li, Y., Xia, Y. L., Ai, S. M., Liang, J., Sang, P., Ji, X. L., & Liu, S. Q. (2016). Insights into protein–ligand interactions: mechanisms, models, and methods. International journal of molecular sciences, 17(2), 144. https://doi.org/10.3390/ijms17020144.
Espino, M., Solari, M., Fernández, D. L. A. M., Boiteux, J., Gómez, M. R., & Silva, M. F. (2019). NADES-mediated folk plant extracts as novel antifungal agents against Candida albicans. Journal of pharmaceutical and biomedical analysis, 167(15), 15-20. https://doi.org/10.1016/j.jpba.2019.01.026.
Fernandes, F. H., Batista, R. S. D. A., Medeiros, F. D. D., Santos, F. S., & Medeiros, A. C. (2015). Development of a rapid and simple HPLC-UV method for determination of gallic acid in Schinopsis brasiliensis. Revista Brasileira de Farmacognosia, 25(3), 208-211. https://doi.org/10.1016/j.bjp.2015.05.006 .
Fontenelle, R. O. S., Morais, S. M., Brito, E. H. S., Kerntopf, M. R., Brilhante, R. S. N., Cordeiro, R. A., Tome, 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. Journal of Antimicrobial Chemotherapy, 59(5), 934-940. https://doi.org/10.1093/jac/dkm066.
Funari, C. S., & Ferro, V. O. (2006). Análise de própolis. Ciência e Tecnol. Aliment, 26(1), 171–178. https://doi.org/10.1590/S0101-20612006000100028.
Gobbo-Neto, L., & Lopes, N. P. (2007). Plantas medicinais: fatores de influência no conteúdo de metabólitos secundários. Quim. Nova, 30(2), 374–381. https://doi.org/10.1590/S0100-40422007000200026
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), 1-17. http://www.jcheminf.com/content/4/1/17.
Holetz, F. B., Pessini, G. L., Sanches, N. R., Cortez, D. A. G., Nakamura, C. V., & Dias Filho, B. P. (2002). Screening of some plants used in the Brazilian folk medicine for the treatment of infectious diseases. Memórias do Instituto Oswaldo Cruz, 97(7), 1027-1031. https://doi.org/10.1590/S0074-02762002000700017.
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.
Kannan, R. V., Sumathi, C.S., Balasubramanian, V., & Ramesh, N. (2009). Elementary chemical profiling and antifungal properties of cashew (Anacardium occidentale L.) nuts. Botany Research International, 2(4), 253-257. https://www.researchgate.net/profile/Ramesh-Nachimuthu/publication/237358357.
Lagrouh, F., Dakka, N., & Bakri, Y. (2017). The antifungal activity of Moroccan plants and the mechanism of action of secondary metabolites from plants. Journal de mycologie medicale, 27 (3), 303-311. https://doi.org/10.1016/j.mycmed.2017.04.008.
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.
Li, Q., Mu, Z., Zhao, R., Dahal, G., Viola, R.E., Liu, T., Jin, Q., & Cui, S. (2016) Structural Insights into the Tetrameric State of Aspartate-β-semialdehyde Dehydrogenases from Fungal Species. Scientific reports, 6(1), 1-13. https://doi.org/10.1038/srep21067.
Li, Z. J., Guo, X., Dawuti, G., & Aibai, S. (2015). Antifungal activity of ellagic acid in vitro and in vivo. Phytotherapy Research, 29(7), 1019-1025. https://doi.org/10.1002/ptr.5340.
Luna, M. S. M., De Paula, R. A., Costa, R. B., Dos Anjos, J. V., Da Silva, M. V.; & Correia, M. T. S. (2020). Bioprospection of Libidibia ferrea var. ferrea: Phytochemical properties and antibacterial activity. South African Journal of Botany, 130, 103-108. https://doi.org/10.1016/j.sajb.2019.12.013.
Madikizela, B., Aderogba, M. A., & Van Staden, J. (2013). Isolation and characterization of antimicrobial constituents of Searsia chirindensis L. (Anacardiaceae) leaf extracts. Journal of ethnopharmacology, 150 (2), 609-613. https://doi.org/10.1016/j.jep.2013.09.016.
Matos, F.J.A. Introdução à Fitoquímica Experimental. (2009). 3 ed. Fortaleza: UFC. 150p.
Mendes, F. E. T., Miranda, G. M., Camilo, H. K. V. S.; Lira, R. D. S., Bitu, V. D. C. L., & Souza, C. E. S. (2021). Avaliação da atividade antimicrobiana, antioxidante e citoprotetora da quercetina contra a ação tóxica do cloreto de bário. Research, Society and Development, 10(6), 1-8.
http://dx.doi.org/10.33448/rsd-v10i6.15632.
Mohamed, M. S., Saleh, A. M., Abdel-Farid, I. B., & El-Naggar, S. A. (2016). Growth, hydrolases and ultrastructure of Fusarium oxysporum as affected by phenolic rich extracts from several xerophytic plants. Pesticide biochemistry and physiology, 141, 57-64. https://doi.org/10.1016/j.pestbp.2016.11.007.
Morais, S. M., Silva Lopes, F. F., 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). Research, Society and Development, 10(5), 1-12. http://dx.doi.org/10.33448/rsd-v10i5.14493.
Milenković, D. A., Dimić, D. S., Avdović, E. H., & Marković, Z. S. (2020). Several coumarin derivatives and their Pd (II) complexes as potential inhibitors of the main protease of SARS-CoV-2, an in silico approach. RSC Advances, 10(58), 35099-35108. https://doi.org 10.1039/D0RA07062A
Nachbar RB, Halgren TA (2000) Merck Molecular Force Field. IV. Conformational Energies and Geometries for MMFF94. Journal Computational Chemistry, 17(5-6), 587-651. https://doi.org/10.1002/(SICI)1096-987X.
Nascimento, P. P. S., Ferraz- Carvalho, R. S., Silva, T. S., Araújo, T. A. S., Amorim, E. L. C., Pereira, M. A., & Cavalcanti, I. M. F. (2021). Interaction between bark extract of Anadenanthera colubrina var. cebil (Griseb.) Altschul with antibiotics against methicillin-resistant Staphylococcus aureus (MRSA). Research, Society and Development, 10(6), 1-10. http://dx.doi.org/10.33448/rsd-v10i6.15469.
Neves, A. M., Santos Silva, H., Sousa, E. B., Santos Fontenelle, R. O., Silva, A. C., & Morais, S. M. (2019). Perfil fitoquímico e avaliação da atividade antifúngica da fração hexânica de Mitracarpus baturitensis (Rubiaceae). Essentia-Revista de Cultura, Ciência e Tecnologia da UVA, 20(1), 96-101. https://doi.org/10.36977/ercct.v20i1.241.
Nivheda, k., Sivasakthi, S., Prakash, A., Devipriya, N., & Vadivel, V. (2020). In vitro studies on antioxidant and cyto-protective activities of polyphenol-rich fraction isolated from Mangifera indica leaf. South African Journal of Botany, 130, 396-406. https://doi.org/10.1016/j.sajb.2020.01.019.
Oliveira, V. M., Carraro, E., Auler, M. E., & Khalil, N. M. (2016). Quercetin and rutin as potential agents antifungal against Cryptococcus spp. Brazilian Journal of Biology, 76(4), 1029-1034. https://doi.org/10.1590/1519-6984.07415.
Omoregie, E. S., & Oikeh, E. I. (2015). Comparative studies on the phytochemical composition, phenolic content and antioxidant activities of methanol leaf extracts of Spondias mombin and Polyathia longifolia. Jordan Journal of Biological Sciences, 147(3427), 1-5. https://doi.org/10.12816/0027561.
Palafox-Carlos, H., Yahia, E. M., & González-Aguilar, G. A. (2012). Identification and quantification of major phenolic compounds from mango (Mangifera indica, cv. Ataulfo) fruit by HPLC–DAD–MS/MS-ESI and their individual contribution to the antioxidant activity during ripening. Food chemistry, 135(1), 105-111. https://doi.org/10.1016/j.foodchem.2012.04.103.
Penido, A. B., De Morais, S. M., Ribeiro, A. B., Alves, D. R., Rodrigues, A. L. M., Dos Santos, L. H., & De Menezes, J. E. S. A. (2017). Medicinal plants from northeastern Brazil against Alzheimer’s disease. Evidence-Based Complementary and Alternative Medicine. https://doi.org/10.1155/2017/1753673.
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.
Rahimmalek, M., Afshari, M., Sarfaraz, D., & Miroliaei, M. (2020). Using HPLC and multivariate analyses to investigate variations in the polyphenolic compounds as well as antioxidant and antiglycative activities of some Lamiaceae species native to Iran. Industrial Crops and Products, 154 (112640), 1-9. https://doi.org/10.1016/j.indcrop.2020.112640.
Rodrigues, F. C., Santos, A. T. L., Machado, A. J. T., Bezerra, C. F., Freitas, T. S., Coutinho, H. D. M., Morais-Braga, M. F. B., Bezerra, J. W. A., Duarte, A. E., Kamdem, J. P., Boligon, A. A., Campos, M. M. A., & Barros, L. M. (2019). Chemical composition and anti-Candida potencial of the extracts of Tarenaya spinosa (Jacq.) Raf. (Cleomaceae). Comparative immunology, microbiology and infectious diseases, 64, 14-19. https://doi.org/10.1016/j.cimid.2019.02.005.
Sales, M. D. C., Costa, H. B., Fernandes, P. M. B., Ventura, J. A., & Meira, D. D. (2016). Antifungal activity of plant extracts with potential to control plant pathogens in pineapple. Asian Pacific Journal of Tropical Biomedicine, 6(1), 26-31. https://doi.org/10.1016/j.apjtb.2015.09.026.
Salomon, M. B., Talla, E., Nyemb, J. N., Ngassoum, M. B., Karole, T. T. R.; & Mahmout, Y. (2018). Comparative survey of three processes used for the extraction of total phenol content and total flavonoid content of Anacardium occidentale L. and the assessment of its antioxidant activity. African Journal of Biotechnology, 17 (40), 1265-1273. https://doi.org/10.5897/AJB2017.16294.
Santos, G. H. F., Amaral, A., & Silva, E. B. (2018). Antibacterial activity of irradiated extracts of Anacardium occidentale L. on multiresistant strains of Staphylococcus aureus. Applied Radiation and Isotopes, 140, 327-332. https://doi.org/10.1016/j.apradiso.2018.07.035.
Santos, C. C. D. S., Guilhon, C. C., Moreno, D. S. A., Alviano, C. S., dos Santos Estevam, C., Blank, A. F., & Fernandes, P. D. (2018). Anti-inflammatory, antinociceptive and antioxidant properties of Schinopsis brasiliensis bark. Journal of ethnopharmacology, 213(1), 176-182. https://doi.org/10.1016/j.jep.2017.11.012.
Santos, C. C. S., Masullo, M., Cerulli, A., Mari, A., Estevam, C. D. S., Pizza, C., & Piacente, S. (2017). Isolation of antioxidant phenolics from Schinopsis brasiliensis based on a preliminary LC-MS profiling. Phytochemistry, 140, 45-51. https://doi.org/10.1016/j.phytochem.2017.04.008.
Sampaio, T. I. D. S., Melo, N. C., Paiva, B. T. D. F., Aleluia, G. A. S., Neto, F. L. P. D. S., Silva, H. R. D., Cruz, H. K. R. A. S., Sánchez-Ortiz, B. L., Pineda-Peña, E. A., Balderas, J. L., Navarrete, A., & Carvalho, J. C. T. (2018). Leaves of Spondias mombin L. a traditional anxiolytic and antidepressant: Pharmacological evaluation on zebrafish (Danio rerio). Journal of ethnopharmacology, 224, 563-578. https://doi.org/10.1016/j.jep.2018.05.037.
Singh, R., Singh, S. K., Maharia, R. S., & Garg, A. N. (2015). Identification of new phytoconstituents and antimicrobial activity in stem bark of Mangifera indica (L.). Journal of pharmaceutical and biomedical analysis, 105(25), 150-155. https://doi.org/10.1016/j.jpba.2014.12.010.
Singh, S. K., Tiwari, R. M., Sinha, S. K., Danta, C. C., & Prasad, S. K. (2012). Antimicrobial evaluation of mangiferin and its synthesized analogues. Asian Pacific Journal of Tropical Biomedicine, 2(2), 884-887. https://doi.org/10.1016/S2221-1691(12)60329-3.
Silva, R. A., Liberio, S. A., Amaral, F. M., Nascimento, F. R. F., Torres, L. M. B., Neto, V. M., & Guerra, R. N. M. (2016). Antimicrobial and antioxidant activity of Anacardium occidentale L. flowers in comparison to bark and leaves extracts. Journal of Biosciences and Medicines, 4 (04), 87-89. https://doi.org/10.4236/jbm.2016.44012.
Sousa, C. M. D. M., Silva, H. R. E., Vieira, G. M., Ayres, M. C. C., Da Costa, C. L. S., Araújo, D. S., Cavalcante, L. C. D., Barros, E. D. S., Araújo, P. B. D. M., Brandão, M. S., & Chaves, M. H. (2007). Fenóis totais e atividade antioxidante de cinco plantas medicinais. Quim. Nova, 30(2), 351–355. https://doi.org/10.1590/S0100-40422007000200021.
Temitope, O. O., Ogunmodede, A. F., Fasusi, O. A., Thonda, A. O., & Odufunwa, A. E. (2017). Synergistic Antibacterial and Antifungal Activities of Spondias mombin Extracts and Conventional Antibiotic and Antifungal Agents on Selected Clinical Microorganisms. Scholars Journal of Applied Medical Sciences (SJAMS), 5, (2A), 307-318. https://doi.org/10.21276/sjams.2017.5.2.
Torres, C. A., Zamora, C. M. P., Nuñez, M. B., & Gonzalez, A. M. (2018). In vitro antioxidant, antilipoxygenase and antimicrobial activities of extracts from seven climbing plants belonging to the Bignoniaceae. Journal of integrative medicine, 16(4), 255-262. https://doi.org/10.1016/j.joim.2018.04.009.
Trott, O., & Olson, A. J. (2010). 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.
Yepez, B., Espinosa, M., López, S., & Bolaños, G. (2002). Producing antioxidant fractions from herbaceous matrices by supercritical fluid extraction. Fluid Phase Equilibria, 194(30), 879-884. https://doi.org/10.1016/S0378-3812(01)00707-5.
Yun, J., Lee, H., Ko, H. J., Woo, E. R., & Lee, D. G. (2015). Fungicidal effect of isoquercitrin via inducing membrane disturbance. Biochimica et Biophysica Acta (BBA)-Biomembranes, 1848 (2), 695-701. https://doi.org/10.1016/j.bbamem.2014.11.019.
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.
Ziani, B. E. C., Carocho, M., Abreu, R. M. V., Bachari, K., Alves, M. J., Calhelha, R. C., Talhi, O., Barros, L., & Ferreira, I. C. F. R. (2020). Phenolic profiling, biological activities and In silico studies of Acacia tortilis (Forssk.) Hayne ssp. raddiana extracts. Food Bioscience, 36, 100616. https://doi.org/10.1016/j.fbio.2020.100616
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Andréa Maria Neves; Raquel Oliveira dos Santos Fontenelle; Flávio Silva Lopes; Josilayne de Fátima Souza Mendes; Ana Livya Moreira Rodrigues; Márcia Machado Marinho; Emmanuel Silva Marinho; Selene Maia de Morais
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.
