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Original Research

Antioxidant and anti-inflammatory activities, bioaccessibility, transmembrane transport of major phenolics from selected floral honeys using Caco-2 BBe1 cell model

Yan ZhuaRonghua LiuaLili MatsaHonghui ZhuaTauseef Khanb,c,dJohn Sievenpiperb,c,d,e,fDan RamdathaRong Tsaoa()
Guelph Research and Development Centre, Agriculture and Agri-Food Canada, 93 Stone Road West, Guelph, Ontario N1G 5C9, Canada
Department of Nutritional Sciences, Temerty Faculty of Medicine, University of Toronto, Toronto, Canada
Toronto 3D Knowledge Synthesis and Clinical Trials Unit, Clinical Nutrition, St Michael’s Hospital, Toronto, Ontario, Canada
Clinical Nutrition and Risk Factor Modification Centre, St Michael’s Hospital, Toronto, Ontario, Canada
Division of Endocrinology and Metabolism, St. Michael’s Hospital, Toronto, Ontario, Canada
Li Ka Shing Knowledge Institute, St Michael’s Hospital, Toronto, Ontario, Canada
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Abstract

In the present study, we assessed the antioxidant activity of the phenolic extracts and major phenolic compounds of alfalfa, buckwheat, clover and orange honeys collected in North America using chemical-based and cell-based antioxidant assays (CAA). Cell culture models using Caco-2 BBe1 were established to evaluate the effect of honey phenolics on antioxidant enzyme activities and secretion of interleukin 8 (IL-8). Moreover, bioaccessibility, transmembrane transport and cellular uptake of honey phenolics were also studied. Based on the same quantity of the honey studied, phenolic extract of buckwheat honey showed the highest FRAP, DPPH, ORAC and CAA values, and strongest activity in restoring activities of antioxidant enzymes (GR, SOD and CAT) and in reducing TNF-α-induced IL-8 secretion. Our results showed that compared to the major phenolic component of honey of plant origin, minor phenolics or combination of different phenolic compounds, particularly those derived from propolis, and their phase Ⅱ metabolites may play contribute more to the overall antioxidant and anti-inflammatory effects. Future research will focus on bioavailability of honey phenolics and their metabolites, and the molecular mechanism of the antioxidant, anti-inflammatory activities.

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References

 

Alevia, M., Rasines, S., Cantero, L., Sancho, M.T., Fernández-Muiño, M.A., and Osés, S.M. (2021). Chemical Extraction and Gastrointestinal Digestion of Honey: Influence on Its Antioxidant, Antimicrobial and Anti-Inflammatory Activities. Foods 10(6): 1412.

 

Battino, M., Giampieri, F., Cianciosi, D., Ansary, J., Chen, X., Zhang, D., Gil, E., and Forbes-Hernández, T. (2021). The roles of strawberry and honey phytochemicals on human health: A possible clue on the molecular mechanisms involved in the prevention of oxidative stress and inflammation. Phytomedicine 86: 153170.

 

Bertoncelj, J., Polak, T., Kropf, U., Korošec, M., and Golob, T. (2011). LC-DAD-ESI/MS analysis of flavonoids and abscisic acid with chemometric approach for the classification of Slovenian honey. Food Chem. 127(1): 296–302.

 

Beszterda, M., and Frański, R. (2021). Electrospray ionisation mass spectrometric behaviour of flavonoid 5-O-glucosides and their positional isomers detected in the extracts from the bark of Prunus cerasus L. and Prunus avium L. Phytochem. Anal. 32(3): 433–439.

 

Bloor, S.J., and Mitchell, K.A. (2021). Metabolic products of European-type propolis. Synthesis and analysis of glucuronides and sulfates. J. Ethnopharmacol. 274: 114035.

 

Borrás-Linares, I., Herranz-López, M., Barrajón-Catalán, E., Arráez-Román, D., González-Álvarez, I., Bermejo, M., Fernández Gutiérrez, A., Micol, V., and Segura-Carretero, A. (2015). Permeability Study of Polyphenols Derived from a Phenolic-Enriched Hibiscus sabdariffa Extract by UHPLC-ESI-UHR-Qq-TOF-MS. Int. J. Mol. Sci. 16(8): 18396–411.

 

Chen, Y., Zhang, H., Fan, W., Mats, L., Liu, R., Deng, Z., and Tsao, R. (2021). Anti-Inflammatory Effect and Cellular Transport Mechanism of Phenolics from Common Bean (Phaseolus vulga L.) Milk and Yogurts in Caco-2 Mono- and Caco-2/EA.hy926 Co-Culture Models. J. Agric. Food Chem. 69(5): 1513–1523.

 

Furger, C. (2021). Live Cell Assays for the Assessment of Antioxidant Activities of Plant Extracts. Antioxidants (Basel) 10(6): 944.

 

Gasparrini, M., Afrin, S., Forbes-Hernández, T.Y., Cianciosi, D., ReboredoRodriguez, P., Amici, A., Battino, M., and Giampieri, F. (2018). Protective effects of Manuka honey on LPS-treated RAW 264.7 macrophages. Part 2: Control of oxidative stress induced damage, increase of antioxidant enzyme activities and attenuation of inflammation. Food Chem. Toxicol. 120: 578–587.

 

Giordano, A., Retamal, M., Leyton, F., Martínez, P., Bridi, R., Velásquez, P., and Montenegro, G. (2018). Bioactive polyphenols and antioxidant capacity of Azara petiolaris and Azara integrifolia Honeys. CyTA - J. Food 16(1): 484–489.

 

Hithamani, G., Kizhakayil, D., and Srinivasan, K. (2017). Uptake of phenolic compounds from plant foods in human intestinal Caco-2 cells. J. BioSci. 42(4): 603–611.

 

Li, H., Deng, Z., Liu, R., Loewen, S., and Tsao, R. (2014). Bioaccessibility, in vitro antioxidant activities and in vivo anti-inflammatory activities of a purple tomato (Solanum lycopersicum L.). Food Chem. 159: 353–360.

 

Li, H., Deng, Z.Y., Zhu, H., Hu, C., Liu, R., Young, J.C., and Tsao, R. (2012). Highly pigmented vegetables: Anthocyanin compositions and their role in antioxidant activities. Food Res. Int. 46: 250–259.

 

Machado De-Melo, A.A., Almeida-Muradian, L.B.D., Sancho, M.T., and Pascual-Maté, A. (2018). Composition and properties of Apis mellifera honey: A review. J. Apic. Res. 57(1): 5–37.

 

O’Sullivan, A.M., O’Callaghan, Y.C., O’Connor, T.P., and O’Brien, N.M. (2013). Comparison of the Antioxidant Activity of Commercial Honeys, Before and After In-Vitro Digestion. Pol. J. Food Nutr. Sci. 63(3): 167–171.

 

Poulsen-Silva, E., Gordillo-Fuenzalida, F., Velásquez, P., Llancalahuen, F.M., Carvajal, R., Cabaña-Brunod, M., and Otero, M.C. (2023). Antimicrobial, Antioxidant, and Anti-Inflammatory Properties of Monofloral Honeys from Chile. Antioxidants 12(9): 1785.

 

Ranneh, Y., Akim, A.M., Hamid, H.A., Khazaai, H., Fadel, A., Zakaria, Z.A., Albujja, M., and Bakar, M.F.A. (2021). Honey and its nutritional and anti-inflammatory value. BMC Complementary Med. Ther. 21(1): 30.

 

Rastogi, H., and Jana, S. (2016). Evaluation of physicochemical properties and intestinal permeability of six dietary polyphenols in human intestinal colon adenocarcinoma Caco-2 cells. Eur. J. Drug Metab. Pharma cokinet. 41(1): 33–43.

 

Redan, B.W., Chegeni, M., and Ferruzzi, M.G. (2017). Differentiated Caco-2 cell monolayers exhibit adaptation in the transport and metabolism of flavan-3-ols with chronic exposure to both isolated flavan-3-ols and enriched extracts. Food Funct. 8(1): 111–121.

 

Rodriguez-Mateos, A., Toro-Funes, N., Cifuentes-Gomez, T., Cortese-Krott, M., Heiss, C., and Spencer, J.P.E. (2014). Uptake and metabolism of (-)-epicatechin in endothelial cells. Arch. Biochem. Biophys. 559: 17–23.

 

Ruiz-Ruiz, J.C., Matus-Basto, A.J., Acereto-Escoffié, P., and Segura-Campos, M.R. (2017). Antioxidant and anti-inflammatory activities of phenolic compounds isolated from Melipona beecheii honey. Food Agric. Im munol. 28(6): 1424–1437.

 

Sanchez-Bridge, B., Lévèques, A., Li, H., Bertschy, E., Patin, A., and Actis Goretta, L. (2015). Modulation of (–)-Epicatechin Metabolism by Coadministration with Other Polyphenols in Caco-2 Cell Model. Drug Metab. Dispos. 43(1): 9.

 

Seraglio, S.K.T., Valese, A.C., Daguer, H., Bergamo, G., Azevedo, M.S., Nehring, P., Gonzaga, L.V., Fett, R., and Costa, A.C.O. (2017). Effect of in vitro gastrointestinal digestion on the bioaccessibility of phenolic compounds, minerals, and antioxidant capacity of Mimosa scabrella Bentham honeydew honeys. Food Res. Int. 99: 670–678.

 

Shen, S., Wang, J., Chen, X., Liu, T., Zhuo, Q., and Zhang, S.Q. (2019). Evaluation of cellular antioxidant components of honeys using UPLC-MS/MS and HPLC-FLD based on the quantitative composition-activity relationship. Food Chem. 293: 169–177.

 

Silva, B., Biluca, F.C., Gonzaga, L.V., Fett, R., Dalmarco, E.M., Caon, T., and Costa, A.C.O. (2021). In vitro anti-inflammatory properties of honey flavonoids: A review. Food Res. Int. 141: 110086.

 

Sultana, S., Foster, K., Lim, L.Y., Hammer, K., and Locher, C. (2022). A Review of the Phytochemistry and Bioactivity of Clover Honeys (Trifolium spp.). Foods 11(13): 1901.

 

Sun, L.-P., Shi, F.-F., Zhang, W.-W., Zhang, Z.-H., and Wang, K. (2020). Antioxidant and Anti-Inflammatory Activities of Safflower (Carthamus tinctorius L.) Honey Extract. Foods 9(8): 1039.

 

Tanleque-Alberto, F., Juan-Borrás, M., and Escriche, I. (2020). Antioxidant characteristics of honey from Mozambique based on specific flavonoids and phenolic acid compounds. J. Food Compos. Anal. 86: 103377.

 

Tel-Çayan, G., Çiftçi, B.H., Taş-Küçükaydın, M., Temel, Y., Çayan, F., Küçükaydın, S., and Duru, M.E. (2023). Citrus Honeys from Three Different Regions of Turkey: HPLC-DAD Profiling and in Vitro Enzyme Inhibition, Antioxidant, Anti-Inflammatory and Antimicrobial Properties with Chemometric Study. Chem. Biodiversity 20(9): e202300990.

 

Tomás-Barberán, F.A., Martos, I., Ferreres, F., Radovic, B.S., and Anklam, E. (2001). HPLC flavonoid profiles as markers for the botanical origin of European unifloral honeys. J. Sci. Food Agric. 81: 485–496.

 

Wang, X., Chen, Y., Hu, Y., Zhou, J., Chen, L., and Lu, X. (2022). Systematic Review of the Characteristic Markers in Honey of Various Botanical, Geographic, and Entomological Origins. ACS Food Sci. Technol. 2: 206–220.

 

Yu, W., Sun, F., Xu, R., Cui, M., Liu, Y., Xie, Q., Guo, L., Kong, C., Li, X., Guo, X., and Luo, L. (2023). Chemical composition and anti-inflammatory activities of Castanopsis honey. Food Funct. 14(1): 250–261.

 

Zammit Young, G.W., and Blundell, R. (2023). A review on the phytochemical composition and health applications of honey. Heliyon 9(2): e12507.

 

Zhang, H., Hassan, Y.I., Liu, R., Mats, L., Yang, C., Liu, C., and Tsao, R. (2020). Molecular Mechanisms Underlying the Absorption of Aglycone and Glycosidic Flavonoids in a Caco-2 BBe1 Cell Model. ACS Omega 5(19): 10782–10793.

 

Zhang, H., Hassan, Y.I., Renaud, J., Liu, R., Yang, C., Sun, Y., and Tsao, R. (2017). Bioaccessibility, bioavailability, and anti-inflammatory effects of anthocyanins from purple root vegetables using mono- and co-culture cell models. Mol. Nutr. Food Res. 61(10): 1600928.

 

Zhu, Y., Liu, R., Mats, L., Zhu, H., Roasa, J., Khan, T., Ahmed, A., Brummer, Y., Cui, S., Sievenpiper, J., Ramdath, D.D., and Tsao, R. (2024). A comprehensive characterization of phenolics, amino acids and other minor bioactives of selected honeys and identification of botanical origin markers. J. Food Bioact. 25: 25–41.

Journal of Food Bioactives
Pages 76-87
Cite this article:
Zhu Y, Liu R, Mats L, et al. Antioxidant and anti-inflammatory activities, bioaccessibility, transmembrane transport of major phenolics from selected floral honeys using Caco-2 BBe1 cell model. Journal of Food Bioactives, 2024, 28: 76-87. https://doi.org/10.26599/JFB.2024.95028398
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