Abstract
Artichoke has long been served as medicinal plant in Mediterranean area and central Asia. But very few information about their function on inhibiting the digestive enzyme and AGEs formation can be found. In order to expand the health benefit of the artichoke planted in Taiwan, we investigate the inhibitory activities of its fruits and leaves at different maturity stages on lipase, α-amylase, α-glucosidase and AGEs formation. Results showed that, young leaf (YL) exhibited the best inhibition of all the digestive enzymes and AGEs formation. For example, the IC50 of lipase and AGEs formation was 28.53 µg/µL and 7.09 µg/µL, respectively. The HPLC and PCA analysis further revealed that samples were clearly separated based on fruits and leaves maturity stages (a total variance of 91%). The major contribution factor is AGEs inhibition (F = 1156.30) followed by α-amylase inhibition (F = 292.66) and DPPH scavenging (F = 203.53). Among the phenolics, the amount of chlorogenic acid and Ethyl-3,4-dihydroxybenzoate were the most abundant, and account for 87.90% and 5.78%, respectively. The high correlation between these compounds and the inhibition of digestive enzymes and AGEs formation, indicating that fruits and leaves of artichoke planted in Taiwan can be a potential material of anti-diabetic and anti-obesity health supplements.
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Data available from the corresponding authors on reasonable request.
References
López-Salas, L., Borrás-Linares, I., Quintin, D., García-Gomez, P., Giménez-Martínez, R., Segura-Carretero, A., Lozano-Sánchez, J.: Artichoke by-products as natural source of phenolic food ingredient. Appl. Sci. 11, 3788 (2021)
Aune, D., Giovannucci, E., Boffetta, P., Fadnes, L.T., Keum, N., Norat, T., Greenwood, D.C., Riboli, E., Vatten, L.J., Tonstad, S.: Fruit and vegetable intake and the risk of cardiovascular disease, total cancer and all-cause mortality-A systematic review and dose-response meta-analysis of prospective studies. Int. J. Epidemiol. 46, 1029–1056 (2017). doi:https://doi.org/10.1093/ije/dyw319
Noriega-Rodríguez, D., Soto-Maldonado, C., Torres-Alarcón, C., Pastrana-Castro, L., Weinstein-Oppenheimer, C., Zúñiga-Hansen, M.E.: Valorization of globe artichoke (Cynara scolymus) agro-industrial discards, obtaining an extract with a selective effect on viability of cancer cell lines. Processes. 8, 715 (2020)
Órbenes, G., Rodríguez-Seoane, P., Torres, M.D., Chamy, R., Zúñiga, M.E., Domínguez, H.: Valorization of artichoke industrial by-products using green extraction technologies: formulation of hydrogels in combination with paulownia extracts. Molecules 26, 4386 (2021)
Doria, E., Boncompagni, E., Marra, A., Dossena, M., Verri, M., Buonocore, D.: Polyphenols extraction from vegetable wastes using a green and sustainable method. Front. Nutr. 5, 1–7 (2021)
Ribeiro, T.B., Voss, G.B., Coelho, M.C., Pintado, M.E.: Food waste and by-product valorization as an integrated approach with zero waste: future challenges. In: Bhat, R. (ed.) Future foods, pp. 569–596. Academic Press, Cambridge (2022)
El Sayed, A.M., Hussein, R., Motaal, A.A., Fouad, M.A., Aziz, M.A., El-Sayed, A.: Artichoke edible parts are hepatoprotective as commercial leaf preparation. Revista Brasileira de Farmacognosia. 28, 165–178 (2018)
Rocchetti, G., Lucini, L., Corrado, G., Colla, G., Cardarelli, M., Pascale, S.D., Rouphael, Y.: Phytochemical profile, mineral content, and bioactive compounds in leaves of seed-propagated artichoke hybrid cultivars. Molecules. 25, 3795 (2020)
Mahboubi, M.: Cynara scolymus (artichoke) and its efficacy in management of obesity. Bull. Fac. Pharm. Cairo Univ. 56, 115–120 (2018)
Spínola, V., Castilho, P.C.: Evaluation of Asteraceae herbal extracts in the management of diabetes and obesity. Contribution of caffeoylquinic acids on the inhibition of digestive enzymes activity and formation of advanced glycation end-products (in vitro). Phytochemistry. 143, 29–35 (2017)
Wu, D.-T., Nie, X.-R., Shen, D.-D., Li, H.-Y., Zhao, L., Zhang, Q., Lin, D.-R., Qin, W.: Phenolic compounds, antioxidant activities, and inhibitory effects on digestive enzymes of different cultivars of okra (Abelmoschus esculentus). Molecules. 25, 1276 (2020)
Zhang, X., Jia, Y., Ma, Y., Cheng, G., Cai, S.: Phenolic composition, antioxidant properties, and inhibition toward digestive enzymes with molecular docking analysis of different fractions from Prinsepia utilis royle fruits. Molecules. 23, 3373 (2018)
Lu, Y., Tian, C., Gao, C., Wang, B., Yang, W., Kong, X., Chai, L., Chen, G., Yin, X., He, Y.: -h.: Phenolic composition, antioxidant capacity and inhibitory effects on α-glucosidase and lipase of immature faba bean seeds. Int. J. Food Prope. 21, 2366–2377 (2018)
Chen, J.-Y., Sridhar, K., Tsai, P.-J.: Anti-glycation and inhibition of starch hydrolyzing enzymes by enzymatically hydrolysed djulis (Chenopodium formosanum Koidz.) Hull, leaf and seedling. Int. J. Food Sci. Technol. 56, 6601–6610 (2021)
Ruiz, H.H., Ramasamy, R., Schmidt, A.M.: Advanced glycation end products: building on the concept of the “common soil” in metabolic disease. Endocrinology 161, 1–10 (2019)
Nguyen, T.M.C., Gavahian, M., Tsai, P.-J.: Ultrasound-assisted extraction of Gac (Momordica cochinchinensis Spreng.) Leaves: effect of maturity stage on phytochemicals and carbohydrate-hydrolyzing enzymes inhibitory activity. Ital. J. Food Sci 33, 34–42 (2021)
Cortez, J., Faicán, M., Pirovani, M., Piagentini, A.: Determination of polyphenols in fruits added with vitamin C: methodology to improve the specificity of the Folin-Ciocalteu test. Revista Iberoamericana de Tecnologia Postcosecha 19, 147–158 (2018)
Chang, C.-C., Yang, M.-H., Wen, H.-M., Chern, J.-C.: Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J. Food Drug Anal. 10, 178–182 (2002)
Wong, C.-C., Li, H.-B., Cheng, K.-W., Chen, F.: A systematic survey of antioxidant activity of 30 chinese medicinal plants using the ferric reducing antioxidant power assay. Food Chem. 97, 705–711 (2006)
Jo, Y.H., Kim, S.B., Liu, Q., Do, S.-G., Hwang, B.Y., Lee, M.K.: Comparison of pancreatic lipase inhibitory isoflavonoids from unripe and ripe fruits of Cudrania tricuspidata. PloS One. 12, e0172069 (2017)
Aleixandre, A., Gil, J.V., Sineiro, J., Rosell, C.M.: Understanding phenolic acids inhibition of α-amylase and α-glucosidase and influence of reaction conditions. Food Chem. 372, 131231 (2022)
Wang, C., Li, W., Chen, Z., Gao, X., Yuan, G., Pan, Y., Chen, H.: Effects of simulated gastrointestinal digestion in vitro on the chemical properties, antioxidant activity, α-amylase and α-glucosidase inhibitory activity of polysaccharides from Inonotus obliquus. Food Res. Int. 103, 280–288 (2018)
Jaradat, N., Zaid, A.N., Hussein, F., Zaqzouq, M., Aljammal, H., Ayesh, O.: Anti-lipase potential of the organic and aqueous extracts of ten traditional edible and medicinal plants in Palestine: a comparison study with Orlistat. Medicines 4, 89 (2017)
Dechakhamphu, A., Wongchum, N.: Screening for anti-pancreatic lipase properties of 28 traditional thai medicinal herbs. Asian Pac. J. Trop. Biomed. 5, 1042–1045 (2015)
Olaokun, O.O., McGaw, L.J., Eloff, J.N., Naidoo, V.: Evaluation of the inhibition of carbohydrate hydrolysing enzymes, antioxidant activity and polyphenolic content of extracts of ten african Ficus species (Moraceae) used traditionally to treat diabetes. BMC Complement. Altern. Med. 13, 94 (2013)
Nadeem, M., Zeb, A.: Impact of maturity on phenolic composition and antioxidant activity of medicinally important leaves of Ficus carica L. Physiol. Mol. Biology Plants. 24, 881–887 (2018)
Brahem, M., Eder, S., Renard, C.M.G.C., Loonis, M., Le Bourvellec, C.: Effect of maturity on the phenolic compositions of pear juice and cell wall effects on procyanidins transfer. LWT. 85, 380–384 (2017)
Kim, J., Jeong, I.-H., Kim, C.-S., Lee, Y.M., Kim, J.M., Kim, J.S.: Chlorogenic acid inhibits the formation of advanced glycation end products and associated protein cross-linking. Arch. Pharm. Res. 34, 495–500 (2011)
Bustos, A.-S., Håkansson, A., Linares-Pastén, J.A., Nilsson, L.: Interaction between myricetin aggregates and lipase under simplified intestinal conditions. Foods. 9, 777 (2020)
Qiu, X.-L., Zhang, Q.-F.: Chemical profile and pancreatic lipase inhibitory activity of Sinobambusa tootsik (Sieb.) Makino leaves. PeerJ. 7, e7765–e7765 (2019)
Martinez-Gonzalez, A.I., Díaz-Sánchez, Ã.G., Rosa, L.A., Vargas-Requena, C.L., Bustos-Jaimes, I., Alvarez-Parrilla, E.: Polyphenolic compounds and digestive enzymes: In vitro non-covalent interactions. Molecules 22, 669 (2017)
Acknowledgements
The authors are grateful to the National Pingtung University of Science and Technology, Pingtung, Taiwan for providing research facilities. Also, we would like to thank Taiwan Tian Jian Biotechnology Co. Ltd., Nantou, Taiwan for providing partial financial support.
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Ye, QM., Sridhar, K. & Tsai, PJ. Artichoke (Cynara scolymus L.) Fruits and Leaves at Different Maturity Stages can Inhibit Digestive Enzymes and Formation of Advanced Glycation End-Products (AGEs). Waste Biomass Valor 14, 3445–3454 (2023). https://doi.org/10.1007/s12649-023-02114-7
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DOI: https://doi.org/10.1007/s12649-023-02114-7