Fermented dairy beverage added with clove essential oil modulates oxygen reactive species (ROS) levels: an in silico, in vitro, and in vivo approach
Keywords:Syzygium aromaticum; Visceral adipose tissue; Superoxide dismutase; Catalase; Glutathione peroxidase.
This study aimed at investigating the effect of fermented dairy beverage with clove essential oil (CEO) on the levels of reactive oxygen species (ROS) through endogenous enzymes superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPx). For this, bioinformatic analysis was performed using the Genecards and String platforms. Headspace was used to analyze and confirm the compounds at low concentrations. Antioxidant activity was analyzed using the DPPH free radical sequestration method. For analysis of antioxidant activity, twenty-four male Swiss mice were divided into three groups and submitted histopathological analysis, analysis of CAT, SOD,GPx transcripts, and CAT and SOD enzyme activity in visceral adipose tissue were evaluated.The leader genes found were PIK3CD, PIK3CB, AKT1, and PIK3CA, as they had the highest WNL values. The beverage containing CEO showed higher antioxidant activity, with free radical scavenging capacity above 80%. In the in vivo analyses, it was possible to verify a reduction in the average adipocyte area size (μm2) between the groups that received fermented dairy beverage. Although functional studies have shown that the antioxidant enzymes, CAT and SOD, showed similar concentrations in visceral adipose tissue of the three groups, the expression levels of GPx1, CAT, and SOD were higher in group 2. Surprisingly, the group 3, that received the fermented dairy beverage with CEO had the lowest SOD concentration (p <0.05). Therefore, the antioxidant mechanism of the CEO can be mediated by the activation of the cell survival pathway PI3K/Akt and modulation of SOD1 and CAT enzymes by means of ROS reduction.
Aebi, H. (1984).  Catalase in vitro (pp. 121–126). https://doi.org/10.1016/S0076-6879(84)05016-3
Aguiar, M. C. S., Silvério, F. O., de Pinho, G. P., Lopes, P. S. N., Fidêncio, P. H., & Ventura, S. J. (2014). Volatile compounds from fruits of Butia capitata at different stages of maturity and storage. Food Research International, 62, 1095–1099. https://doi.org/10.1016/j.foodres.2014.05.039
Andrade, J. M. O., Barcala-Jorge, A. S., Batista-Jorge, G. C., Paraíso, A. F., Freitas, K. M. de, Lelis, D. de F., Guimarães, A. L. S., de Paula, A. M. B., & Santos, S. H. S. (2019). Effect of resveratrol on expression of genes involved thermogenesis in mice and humans. Biomedicine & Pharmacotherapy, 112, 108634. https://doi.org/10.1016/j.biopha.2019.108634
Baldissera, A. C., Betta, F. Della, Penna, A. L. B., & Lindner, J. D. D. (2011). Alimentos funcionais: uma nova fronteira para o desenvolvimento de bebidas protéicas a base de soro de leite. Semina: Ciências Agrárias, 32(4), 1497–1512. https://doi.org/10.5433/1679-0359.2011v32n4p1497
Bannister, J. V., & Calabrese, L. (2006). Assays for Superoxide Dismutase (pp. 279–312). https://doi.org/10.1002/9780470110539.ch5
Brasil. (2005). Ministério da Agricultura Pecuária e Abastecimento. Instrução Normativa n.o 16, de 23 de agosto de 2005. Aprova o regulamento Técnico de Identidade e Qualidade de Bebidas Láctea. Diário Oficial Da República Federativa Do Brasil. https://www2.cead.ufv.br/sgal/files/apoio/legislacao/legislacao6.pdf
Darvishi, E., Omidi, M., Bushehri, A. A. S., Golshani, A., & Smith, M. L. (2013). The Antifungal Eugenol Perturbs Dual Aromatic and Branched-Chain Amino Acid Permeases in the Cytoplasmic Membrane of Yeast. PLoS ONE, 8(10), e76028. https://doi.org/10.1371/journal.pone.0076028
Farias, P. K. S. (2016). Elaboração de bebida láctea fermentada com adição de óleo essencial. Instituto de Ciências Agrárias - Universidade Federal de Minas Gerais(ICA-UFMG).
Gokila Vani, M., Kumar, K. J. S., Liao, J.-W., Chien, S.-C., Mau, J.-L., Chiang, S.-S., Lin, C.-C., Kuo, Y.-H., & Wang, S.-Y. (2013). Antcin C from Antrodia cinnamomea Protects Liver Cells Against Free Radical-Induced Oxidative Stress and Apoptosis In Vitro and In Vivo through Nrf2-Dependent Mechanism. Evidence-Based Complementary and Alternative Medicine, 2013, 1–17. https://doi.org/10.1155/2013/296082
Kamatou, G. P., Vermaak, I., & Viljoen, A. M. (2012). Eugenol—From the Remote Maluku Islands to the International Market Place: A Review of a Remarkable and Versatile Molecule. Molecules, 17(6), 6953–6981. https://doi.org/10.3390/molecules17066953
Lawlor, M. A., & Alessi, D. R. (2001). PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? Journal of Cell Science, 114(Pt 16), 2903–2910. http://www.ncbi.nlm.nih.gov/pubmed/11686294
Le Lay, S., Simard, G., Martinez, M. C., & Andriantsitohaina, R. (2014). Oxidative Stress and Metabolic Pathologies: From an Adipocentric Point of View. Oxidative Medicine and Cellular Longevity, 2014, 1–18. https://doi.org/10.1155/2014/908539
Liu, X.-M., Peyton, K. J., Shebib, A. R., Wang, H., & Durante, W. (2011). Compound C stimulates heme oxygenase-1 gene expression via the Nrf2-ARE pathway to preserve human endothelial cell survival. Biochemical Pharmacology, 82(4), 371–379. https://doi.org/10.1016/j.bcp.2011.05.016
Martins, L. B., Oliveira, M. C. de, Menezes-Garcia, Z., Rodrigues, D. F., Lana, J. P., Vieira, L. Q., Teixeira, M. M., & Ferreira, A. V. M. (2018). Paradoxical role of tumor necrosis factor on metabolic dysfunction and adipose tissue expansion in mice. Nutrition, 50, 1–7. https://doi.org/10.1016/j.nut.2017.07.006
Najgebauer-Lejko, D., Sady, M., Grega, T., & Walczycka, M. (2011). The impact of tea supplementation on microflora, pH and antioxidant capacity of yoghurt. International Dairy Journal, 21(8), 568–574. https://doi.org/10.1016/j.idairyj.2011.03.003
Porta, C., Paglino, C., & Mosca, A. (2014). Targeting PI3K/Akt/mTOR Signaling in Cancer. Frontiers in Oncology, 4. https://doi.org/10.3389/fonc.2014.00064
Prakash, B., Kedia, A., Mishra, P. K., & Dubey, N. K. (2015). Plant essential oils as food preservatives to control moulds, mycotoxin contamination and oxidative deterioration of agri-food commodities – Potentials and challenges. Food Control, 47, 381–391. https://doi.org/10.1016/j.foodcont.2014.07.023
Scherer, R., & Godoy, H. T. (2009). Antioxidant activity index (AAI) by the 2,2-diphenyl-1-picrylhydrazyl method. Food Chemistry, 112(3), 654–658. https://doi.org/10.1016/j.foodchem.2008.06.026
Shimizu, T., Tolcher, A. W., Papadopoulos, K. P., Beeram, M., Rasco, D. W., Smith, L. S., Gunn, S., Smetzer, L., Mays, T. A., Kaiser, B., Wick, M. J., Alvarez, C., Cavazos, A., Mangold, G. L., & Patnaik, A. (2012). The Clinical Effect of the Dual-Targeting Strategy Involving PI3K/AKT/mTOR and RAS/MEK/ERK Pathways in Patients with Advanced Cancer. Clinical Cancer Research, 18(8), 2316–2325. https://doi.org/10.1158/1078-0432.CCR-11-2381
Silva, J. M. de A., Santos, E. M. S., Almeida, A. C. de, Santos, H. O., Farias, P. K. S., Souza, K. S. S., Oliveira, S. P. de, & Santos, P. H. de A. S. (2018). Action of indian cloves (Syzygium aromaticum) in the sensitization of neoplastic cells for radiotherapy: a systematic review of literature. Revista Unimontes Científica, 20, 39–57.
Sordella, R. (2004). Gefitinib-Sensitizing EGFR Mutations in Lung Cancer Activate Anti-Apoptotic Pathways. Science, 305(5687), 1163–1167. https://doi.org/10.1126/science.1101637
Souza, K. S. S., Oliveira, S. P., Duarte, S. M., Brandi, I. V., Santos, S. H. S., Santos, E. M. S., Farias, P. K. S., Santos, H. O., & Almeida, A. C. (2018). Standardization of the methodology for calorimetric analysis of a fermented milk drink. Caderno de Ciências Agrárias, 10(2), 61–63.
Teixeira, B., Marques, A., Ramos, C., Serrano, C., Matos, O., Neng, N. R., Nogueira, J. M. F., Saraiva, J. A., & Nunes, M. L. (2013). Chemical composition and bioactivity of different oregano ( Origanum vulgare ) extracts and essential oil. Journal of the Science of Food and Agriculture, 93(11), 2707–2714. https://doi.org/10.1002/jsfa.6089
Yao, R., & Cooper, G. (1995). Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science, 267(5206), 2003–2006. https://doi.org/10.1126/science.7701324
Zhou, D., Shao, L., & Spitz, D. R. (2014). Reactive Oxygen Species in Normal and Tumor Stem Cells (pp. 1–67). https://doi.org/10.1016/B978-0-12-420117-0.00001-3
Zicker, M. C., Silveira, A. L. M., Lacerda, D. R., Rodrigues, D. F., Oliveira, C. T., de Souza Cordeiro, L. M., Lima, L. C. F., Santos, S. H. S., Teixeira, M. M., & Ferreira, A. V. M. (2019). Virgin coconut oil is effective to treat metabolic and inflammatory dysfunction induced by high refined carbohydrate-containing diet in mice. The Journal of Nutritional Biochemistry, 63, 117–128. https://doi.org/10.1016/j.jnutbio.2018.08.013
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Copyright (c) 2021 Stephanie Pedrosa de Oliveira; Anna Christina de Almeida; Keicy Sandy Silvestre de Souza; Sérgio Henrique Sousa Santos; Eliane Macedo Sobrinho Santos; Igor Viana Brandi; Francine Souza Alves Fonseca; Paula Karoline Soares Farias; João Matheus de Almeida Silva; Luis Paulo Oliveira; Victor Hugo Dantas Guimarães; Cintya Neves Souza; Laura Francielle Ferreira Borges; Raphael Rodrigues Porto; Pedro Henrique Almeida Souto Santos; Hércules Otacilio Santos
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