Effects of phenolic compounds of colored wheats on colorectal cancer cell lines
Main Article Content
Keywords
blue wheat bran, colorectal cancer cells, free and bound phenolic, HCT-116, HT-29, purple wheat bran, red wheat bran
Abstract
In this study, the different colored wheat brans were analyzed and compared for phenolic content (PC), phenolic compositions, and the total antioxidant capacity (TEAC) with methods based on the ability to eliminate radicals of 2,2'-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS), 2,2-diphenyl-1-(2,4,6-trinitrophenyl) hydrazyl (DPPH), and anthocyanin compositions. This study also aims to characterize the bioactive components of wheat grain genotypes as well as to test the protective and rescuer effects of their extracts on colorectal cancer (CRC) cell lines. PCs in the bound insoluble fraction of red wheat bran, blue wheat bran, and purple wheat bran were determined as 369.60, 446.95, and 486.79 mg gallic acid equivalents (GAE)/100 g wheat bran, respectively, while strong relationships were detected between PC and antioxidant activity (DPPH and ABTS) results. HPLC analysis of phenolic extracts demonstrated that ferulic acid was determined as the dominant phenolic acid in the bound fractions of red, purple, and blue wheats. In the free fractions, p-coumaric acid (11.55 µg/100 g wheat bran) was the dominant phenolic acid for red wheat bran, whereas ellagic acid (14.72 and 11.55 µg/100 g wheat bran) was the highest phenolic acid for purple and blue wheat brans, respectively. In bound fractions, ferulic acid was the highest phenolic acid for red (988.39 µg/100 g wheat bran), purple (1948.76 µg/100 g wheat bran), and blue (2263.96 µg/100 g wheat bran) wheat brans. On the other hand, Cyanidin-3-O-glucoside chloride was the predominant anthocyanin in free extracts of purple and blue wheat brans. In line with the antioxidant activities and phenolic acid concentrations, the blue wheat bran extracts increased CRC cell viability nonsignificantly in HT-29 and HCT-116 cell lines, whereas purple wheat bran extract had a significantly higher (P = 0.0361) rescuer effect compared to vehicle control under 50 µM H2O2 concentration. In conclusion, the in vitro data here show that blue and purple wheat brans are posing a novel means to increase the defense of cells against oxidative stress and cell death.
References
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Chen, W., Muüller, D., Richling, E. and Wink, M., 2013. Anthocyanin-rich purple wheat prolongs the life span of Caenorhabditis elegans probably by activating the DAF-16/FOXO transcription factor. Journal of Agricultural and Food Chemistry 61(12): 3047–3053. 10.1021/jf3054643
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Eroğlu, C., Seçme, M., Bağcı, G. and Dodurga, Y., 2015. Assessment of the anticancer mechanism of ferulic acid via cell cycle and apoptotic pathways in human prostate cancer cell lines. Tumor Biology 36: 9437–9446. 10.1007/s13277-015-3689-3
Garg, M., Chawla, M., Chunduri, V., Kumar, R., Sharma, S., Sharma, N.K., Kaur, N., Kumar, A., Mundey, J.K., Saini, M.K. and Singh, S.P., 2016. Transfer of grain colors to elite wheat cultivars and their characterization. Journal of Cereal Science 71: 138–144. 10.1016/j.jcs.2016.08.004
Gordeeva, E., Badaeva, E., Yudina, R., Shchukina, L., Shoeva, O. and Khlestkina, E., 2019. Marker-assisted development of a blue-grained substitution line carrying the Thinopyrum ponticum chromosome 4Th(4D) in the spring bread wheat Saratovskaya 29 background. Agronomy 9(11): 723. 10.3390/agronomy9110723
Hosseinian, F.S., Li, W. and Beta, T., 2008. Measurement of anthocyanins and other phytochemicals in purple wheat. Food Chemistry 109(4): 916–924. 10.1016/j.foodchem.2007.12.083
Hou, Y., Yang, J., Zhao, G. and Yuan, Y., 2004. Ferulic acid inhibits endothelial cell proliferation through NO down-regulating ERK1/2 pathway. Journal of Cellular Biochemistry 93(6): 1203–1209. 10.1002/jcb.20281
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Lachman, J., Martinek, P., Kotíková, Z., Orsák, M. and Šulc, M., 2017. Genetics and chemistry of pigments in wheat grain–a review. Journal of Cereal Science 74: 145–154. 10.1016/j.jcs.2017.02.007
Li, W., Shan, F., Sun, S., Corke, H. and Beta, T., 2005. Free radical scavenging properties and phenolic content of Chinese black-grained wheat. Journal of Agricultural and Food Chemistry 53(22), 8533–8536. 10.1021/jf051634y
Liu, Q., Qiu, Y. and Beta, T., 2010. Comparison of antioxidant activities of different colored wheat grains and analysis of phenolic compounds. Journal of Agricultural and Food Chemistry 58(16): 9235–9241. 10.1021/jf101700s
Liyana-Pathirana, C.M. and Shahidi, F., 2006. Importance of insoluble--bound phenolics to antioxidant properties of wheat. Journal of Agricultural and Food Chemistry 54(4): 1256–1264. 10.1021/jf052556h
Liyana-Pathirana, C.M. and Shahidi, F., 2007. The antioxidant potential of milling fractions from breadwheat and durum. Journal of Cereal Science 45(3): 238–247. 10.1016/j.jcs.2006.08.007
Ma, D., Li, Y., Zhang, J., Wang, C., Qin, H., Ding, H., Xie, Y. and Guo, T., 2016. Accumulation of phenolic compounds and expression profiles of phenolic acid biosynthesis-related genes in developing grains of white, purple, and red wheat. Frontiers in Plant Science 7: 528. 10.3389/fpls.2016.00528
Mazewski, C. and Gonzalez de Mejia, E., 2018. Impact of anthocyanins on colorectal cancer. In: Advances in plant phenolics: from chemistry to human health. American Chemical Society, pp. 339–370. 10.1021/bk-2018-1286.ch019
Mazewski, C., Liang, K. and de Mejia, E.G., 2017. Comparison of the inhibitory potential of anthocyanin-rich plant extracts on colon cancer cell proliferation and their mechanism of action in vitro. The FASEB Journal 31(S1): 300–307. 10.1096/fasebj.31.1_supplement.300.7
Mazewski, C., Liang, K. and Gonzalez de Mejia, E., 2018. Comparison of the effect of chemical composition of anthocyanin--rich plant extracts on colon cancer cell proliferation and their potential mechanism of action using in vitro, in silico, and biochemical assays. Food Chemistry 242: 378–388. 10.1016/j.foodchem.2017.09.086
Mazewski, C.E., 2019. Inhibitory potential of anthocyanins and anthocyanin-rich extracts on colorectal cancer progression through apoptosis, angiogenesis, and immune response effects. Available at: https://hdl.handle.net/2142/105188
Ransy, C., Vaz, C., Lombès, A. and Bouillaud, F., 2020. Use of H(2)O(2) to cause oxidative stress, the catalase issue. International Journal of Molecular Sciences 21(23), 9149. 10.3390/ijms21239149
Rice-Evans, C.A., Miller, N.J. and Paganga, G., 1996. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radical Biology and Medicine 20(7): 933–956. 10.1016/0891-5849(95)02227-9
Roy, N., Narayanankutty, A., Nazeem, P., Valsalan, R., Babu, T. and Mathew, D., 2016. Plant phenolics ferulic acid and p-coumaric acid inhibit colorectal cancer cell proliferation through EGFR down-regulation. Asian Pacific Journal of Cancer Prevention 17(8): 4019–4023. 10.14456/apjcp.2016.208/APJCP.2016.17.8.4019
Saini, P., Kumar, N., Kumar, S., Mwaurah, P.W., Panghal, A., Attkan, A.K., Singh, V.K., Garg, M.K. and Singh, V., 2021. Bioactive compounds, nutritional benefits and food applications of colored wheat: a comprehensive review. Critical Reviews in Food Science and Nutrition 61(19): 3197–3210. 10.1080/10408398.2020.1793727
Serpen, A., Goükmen, V., Karagoüz, A. and Koüksel, H., 2008. Phytochemical quantification and total antioxidant capacities of emmer (Triticum dicoccon Schrank) and einkorn (Triticum monococcum L.) wheat landraces. Journal of Agricultural and Food Chemistry 56(16): 7285–7292. 10.1021/jf8010855
Shamanin, V.P., Tekin-Cakmak, Z.H., Gordeeva, E.I., Karasu, S., Pototskaya, I., Chursin, A.S., Pozherukova, V.E., Ozulku, G., Morgounov, A.I., Sagdic, O. and Koksel, H., 2022. Antioxidant capacity and profiles of phenolic acids in various genotypes of purple wheat. Foods 11(16): 2515. 10.3390/foods11162515
Sharma, S., Chunduri, V., Kumar, A., Kumar, R., Khare, P., Kondepudi, K.K., Bishnoi, M. and Garg, M., 2018. Anthocyanin biofortified colored wheat: nutritional and functional characterization. PLoS One 13(4): e0194367. 10.1371/journal.pone.0194367
Sharma, A., Shahzad, B., Rehman, A., Bhardwaj, R., Landi, M. and Zheng, B., 2019. Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules 24(13): 2452. 10.3390/molecules24132452
Sharma, N., Tiwari, V., Vats, S., Kumari, A., Chunduri, V., Kaur, S., Kapoor, P. and Garg, M., 2020. Evaluation of anthocyanin content, antioxidant potential and antimicrobial activity of black, purple and blue colored wheat flour and wheat-grass juice against common human pathogens. Molecules 25(24): 5785. 10.3390/molecules25245785
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