Phytochemical Composition, Antioxidant Activity, and Anticancer Effects of Root and Sprout Extracts of Quinoa (Chenopodium quinoa willd.) on AGS Gastric Cancer Cells
Subject Areas : Phytochemistry
Fatemeh Shirali
1
,
سیّد ابراهیم سیفتی
2
1 - Department of Arid Land and Desert Management, School of Natural Resources and Desert Studies, Yazd University, Yazd, Iran
2 - Assistant Professor of Biotechnology, Department of Natural Resources and Desert Studies, Yazd University, Yazd, Iran
Keywords: Cytotoxic effects, MTT assay, Titicaca, Flavonoid, Saponins,
Abstract :
This study aimed to investigate the phytochemical composition, antioxidant activity, and anticancer effects of root and sprout samples from Multi-hued Bulk, Black, and Titicaca Quinoa varieties (Chenopodium quinoa willd.) on Human Gastric Adenocarcinoma Cell Line (AGS). These varieties were cultivated using a complete randomized block design with four replications in arid and semi-arid regions of Iran (research field of Yazd University). Root samples were harvested before seed filling from a soil depth of 30 cm. Once the seed germination and filling stages were complete, 100 g of seeds from each variety were randomly selected without hulling to produce sprouts. The highest saponin contents (mg/g dry weight) were observed in the Black root (24.4), followed by the Titicaca root (7.1). The lowest saponin content (0.6) was found in the Black sprout. The phytochemical composition, and antioxidant activity of the hydroethanolic (80:20) extract (obtained using the Soxhlet method), at 100, 250, 500, and 1000 mg/mL were evaluated for root and sprout samples of all three varieties. Based on the results, the Black and Titicaca sprout extract had significantly higher total phenolic (172.68 mgGAE/gDW) and flavonoid (128.17 mgQ/gDW) contents, as well as antioxidant capacity at 1000 mg/mL compared to the corresponding samples from the Multi-hued Bulk variety and the root samples of all three varieties. The lowest and highest DPPH IC50 value was observed in the Black sprout and Multi-hued Bulk root extracts (1.11 and 3.15 mg/mL, respictively). The average cell viability of AGS was observed in the Black sprout extract (33.46) and Titicaca (36.11) varieties at 1000 mg/mL, 72 hours after the treatment, respectively. Findings suggested that the phytochemical and antioxidant properties of Quinoa sprouts, compared to hulled and unhulled seeds of the investigated varieties, could contribute to the development and accessibility of this medicinal plant for patients with cancer.
Agarwal, A., Shaida, B., Rastogi, M., and Singh, N. B. (2023). Food packaging materials with special reference to biopolymers-properties and applications. Chemistry Africa, 6(1): 117-144.
Aliyari, M. A., Motahar, S. F. S., Salami, M., Betti, M., Hosseini, E., Habibi-Kelishomi, Z. and Ghasemi, A. (2022). Structural, functional, and anti-cancer properties of conjugates of quinoa protein isolate and olive leaf polyphenolic extract: Application in production of bread. Food Structure, 33: 100292.
Al-Qabba, M. M., El-Mowafy, M. A., Althwab, S. A., Alfheeaid, H. A., Aljutaily, T., and Barakat, H. (2020). Phenolic profile, antioxidant activity, and ameliorating efficacy of Chenopodium quinoa sprouts against CCl4-induced oxidative stress in rats. Nutrients, 12(10): 2904.
Brand-Williams, W., Cuvelier, M. E. and Berset, C. L. W. T. (1995). Use of a free radical method to evaluate antioxidant activity. LWT-Food science and Technology, 28(1): 25-30.
Darwish, A. M., Al‐Jumayi, H. A. and Elhendy, H. A. (2021). Effect of germination on the nutritional profile of quinoa (Cheopodium quinoa Willd.) seeds and its anti‐anemic potential in Sprague–Dawley male albino rats. Cereal Chemistry, 98(2): 315-327.
Dubal, K. N., Ghorpade, P. N. and Kale, M. V. (2013). Studies on bioactive compounds of Tectaria coadunata (wall. Ex hook. & Grev.) C. Chr. Asian J Pharm Clin Res, 6(2): 186-187.
Eom, J. W., Lim, J. W. and Kim, H. (2023). Lutein Induces Reactive Oxygen Species-Mediated Apoptosis in Gastric Cancer AGS Cells via NADPH Oxidase Activation. Molecules, 28(3): 1178.
Fan, X., Guo, H., Teng, C., Zhang, B., Blecker, C. and Ren, G. (2022). Anti-colon cancer activity of novel peptides isolated from in vitro digestion of quinoa protein in Caco-2 cells. Foods, 11(2): 194.
Galanty, A., Niepsuj, M., Grudzińska, M., Zagrodzki, P., Podolak, I. and Paśko, P. (2022). In the search for novel, isoflavone-rich functional foods—comparative studies of four clover species sprouts and their chemopreventive potential for breast and prostate cancer. Pharmaceuticals, 15(7): 806.
Gawlik-Dziki, U., Świeca, M., Dziki, D., Sęczyk, Ł., Złotek, U., Różyło, R. and Czyż, J. (2014). Anticancer and antioxidant activity of bread enriched with broccoli sprouts. BioMed research international, 1-14
Gómez-Caravaca, A. M., Iafelice, G., Lavini, A., Pulvento, C., Caboni, M. F. and Marconi, E. (2012). Phenolic compounds and saponins in quinoa samples (Chenopodium quinoa Willd.) grown under different saline and nonsaline irrigation regimens. Journal of Agricultural and Food Chemistry, 60(18): 4620–4627.
Han, Y., Chi, J., Zhang, M., Zhang, R., Fan, S., Huang, F. and Xue, K. (2019). Characterization of saponins and phenolic compounds : antioxidant activity and inhibitory e ff ects on α -glucosidase in di ff erent varieties of colored quinoa (Chenopodium quinoa Willd ). Bioscience, Biotechnology, and Biochemistry, 83(11): 2128–2139.
Hosseini, F. S., Karimabad, M. N., Hajizadeh, M. R., Khoshdel, A., Falahati-Pour, S. K., Mirzaei, M. R. and Mahmoodi, M. (2019). Evaluating of induction of apoptosis by Cornus mass L. extract in the gastric carcinoma cell line (AGS). Asian Pacific journal of cancer prevention: APJCP, 20(1): 123.
Hostettamann, K. and Marston, A. (1995). Chemistry and pharmacology of natural products: Saponins. London: Cambridge Universitey Press.
Ilic, M., and Ilic, I. (2022). Epidemiology of stomach cancer. World Journal of Gastroenterology, 28(12): 1187–1203.
Kaijv, M., Sheng, L. and Chao, C. (2006). Antioxidation of flavonoids of Green Rhizome. Food Science, 27(3): 110–115.
Khan, I. H., Javaid, A., Ahmed, D. and Khan, U. (2020). Identification of volatile constituents of ethyl acetate fraction of Chenopodium quinoa roots extract by GC-MS. Int J Biol Biotechnol, 17(1): 17-21.
Koziol, M. J. (1991). Afrosimetric estimation of threshold saponin concentration for bitterness in quinoa (Chenopodium quinoa Willd). Journal of the Science of Food and Agriculture, 54(2): 211–219.
Laus, M., Cataldi, M., Soccio, M., Alfarano, M., Amodio, M., Colelli, G., Flagella, Z. and Pastore, D. (2017). Effect of germination and sprout storage on antioxidant capacity and phenolic content in quinoa (Chenopodium quinoa Willd). Proceedings of the SIBV-SIGA Joint Congress Sustainability of Agricultural Environment: Contributions of Plant Genetics and Physiology, Pisa, Italy, 19–22.
Lim, J. G., Park, H. M. and Yoon, K. S. (2020). Analysis of saponin composition and comparison of the antioxidant activity of various parts of the quinoa plant (Chenopodium quinoa Willd.). Food Science and Nutrition, 8(1): 694–702.
Liu, M., Zhu, K., Yao, Y., Chen, Y., Guo, H., Ren, G., Yang, X. and Li, J. (2020). Antioxidant, anti‐inflammatory, and antitumor activities of phenolic compounds from white, red, and black Chenopodium quinoa seed. Cereal Chemistry, 97(3): 703–713.
Mhada, M., Metougui, M. L., El Hazzam, K., El Kacimi, K. and Yasri, A. (2020). Variations of saponins, minerals and total phenolic compounds due to processing and cooking of quinoa (Chenopodium quinoa Willd.) seeds. Foods, 9(5): 660.
Mohamed, D. A., Fouda, K. A. and Mohamed, R. S. (2019). In vitro Anticancer Activity of Quinoa and Safflower Seeds and Their Preventive Effects on Non-alcoholic Fatty Liver. Pakistan Journal of Biological Sciences: PJBS, 22(8): 383–392.
Nabavi, S. M., Nabavi, S. F. and Ebrahimzadeh, M. A. (2012). Free radical scavenging and antioxidant activities of Dorema aitchisonii. Journal of food and drug analysis, 20(1): 1-8.
Oyaizu, M. (1986). Studies on products of browning reaction antioxidative activities of products of browning reaction prepared from glucosamine. The Japanese Journal of Nutrition and Dietetics, 44(6): 307–315.
Padda, M. S. and Picha, D. H. (2007). Antioxidant activity and phenolic composition in ‘Beauregard’sweetpotato are affected by root size and leaf age. Journal of the American Society for Horticultural Science, 132(4): 447-451.
Paśko, P., Tyszka-Czochara, M., Namieśnik, J., Jastrzębski, Z., Leontowicz, H., Drzewiecki, J. and Gorinstein, S. (2019). Cytotoxic, antioxidant and binding properties of polyphenols from the selected gluten-free pseudocereals and their by-products: In vitro model. Journal of Cereal Science, 87: 325-333.
Paucar‐Menacho, L. M., Martínez‐Villaluenga, C., Duenas, M., Frias, J. and Penas, E. (2018). Response surface optimisation of germination conditions to improve the accumulation of bioactive compounds and the antioxidant activity in quinoa. International Journal of Food Science & Technology, 53(2): 516–524.
Pellegrini, M., Lucas-gonzales, R., Ricci, A. and Fontecha, J. (2018). Chemical, fatty acid, polyphenolic profile, techno-functional and antioxidant properties of flours obtained from quinoa (Chenopodium quinoa Willd ) seeds. Industrial Crops & Products, 111: 38–46.
Pilco-Quesada, S., Tian, Y., Yang, B., Repo-Carrasco-Valencia, R. and Suomela, J. P. (2020). Effects of germination and kilning on the phenolic compounds and nutritional properties of quinoa (Chenopodium quinoa) and kiwicha (Amaranthus caudatus). Journal of Cereal Science, 94: 102996.
Piñuel, L., Boeri, P., Zubillaga, F., Barrio, D. A., Torreta, J., Cruz, A., Vásquez, G., Pinto, A. and Carrillo, W. (2019). Production of white, red and black quinoa (Chenopodium quinoa Willd Var. Real) protein isolates and its hydrolysates in germinated and non-germinated quinoa samples and antioxidant activity evaluation. Plants, 8(8): 257.
Prado, F. E., Boero, C., Gallardo, M. and Gonzalez, J. A. (2000). Effect of NaC1 on Germination, growth, and Soluble Sugar Content in Chenopodium quinoa Wilid. Seeds. Botanical Bulletin of Academia Sinica, 41(1): 27-34.
Ramos-Pacheco, B. S., Choque-Quispe, D., Ligarda-Samanez, C. A., Solano-Reynoso, A. M., Palomino-Rincón, H., Choque-Quispe, Y., and Aiquipa-Pillaca, Á. S. (2024). Effect of Germination on the Physicochemical Properties, Functional Groups, Content of Bioactive Compounds, and Antioxidant Capacity of Different Varieties of Quinoa (Chenopodium quinoa Willd.) Grown in the High Andean Zone of Peru. Foods, 13(3): 417.
Seifati, S. E., Ranaiezadeh, M. R., Daneshmand, F., Karimi Bekr, Z. and Rezaee, M. B. (2024). The Phytochemical Content and Cytotoxic Effects of Quinoa Commercial Cultivars (Chenopodium quinoa Willd.) on MCF7 Cell Line of Breast Cancer. Journal of Medicinal plants and By-product.
Shakuntala, T. S., Krishnan, S. K., Das, P., Sudarshan, K. L., Kotian, C. M., Santhappan, S., Vishwakarma, M. B., Sureshkumar, N. and Mathur, P. (2022). Descriptive Epidemiology of Gastrointestinal Cancers: Results from National Cancer Registry Programme, India. Asian Pacific Journal of Cancer Prevention, 23(2): 409–418.
Shalaby, E. A., and Shanab, S. M. M. (2013). Comparison of DPPH and ABTS assays for determining antioxidant potential of water and methanol extracts of Spirulina platensis. Indian Journal of Geo-Marine Sciences. 42(5): 556-564.
Sigsgaard, L., Jacobsen, S. E. and Christiansen, J. L. (2008). Quinoa, Chenopodium quinoa, provides a new host for native herbivores in northern Europe: Case studies of the moth, Scrobipalpa atriplicella, and the tortoise beetle, Cassida nebulosa. Journal of Insect Science, 8(1): 50-54.
Singh, K. V., and Singh, R. (2016). Quinoa (Chenopodium quinoa Willd), functional superfood for today’s world: A Review. World scientific news, (58): 84-96.
Soland, S. F., and Laima, S. K. (1999). Phenolics and cold tolerance of Brassica napus. Plant Agriculture, 1: 1–5.
Stikić, R. I., Milinčić, D. D., Kostić, A., Jovanović, Z. B., Gašić, U. M., Tešić, Ž. L., Djordjević, N. Z., Savić, S. K., Czekus, B. G. and Pešić, M. B. (2020). Polyphenolic profiles, antioxidant, and in vitro anticancer activities of the seeds of Puno and Titicaca quinoa cultivars. Cereal Chemistry, 97(3): 626–633.
Suárez-Estrella, D., Borgonovo, G., Buratti, S., Ferranti, P., Accardo, F., Pagani, M. A. and Marti, A. (2021). Sprouting of quinoa (Chenopodium quinoa Willd.): Effect on saponin content and relation to the taste and astringency assessed by electronic tongue. Plant Foods for Human Nutrition, 75: 635-641.
Sung, H., Ferlay, J., Siegel, R. L., Laversanne, M., Soerjomataram, I., Jemal, A. and Bray, F. (2021). Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: a cancer journal for clinicians, 71(3): 209-249.
Wang, S., Liu, G., Xie, C., Zhou, Y., Yang, R., Wu, J. and Tu, K. (2024). Metabolomics Analysis of Different Quinoa Cultivars Based on UPLC-ZenoTOF-MS/MS and Investigation into Their Antioxidant Characteristics. Plants, 13(2): 240.
Zhou, X., YUE, T., Wei, Z., Yang, L., Zhang, L., Wu, B. and Peng, P. (2023). Tea-making technology by using quinoa raw materials. Food Science and Technology, 43.
