Abstract
The objective of this study was to investigate the effect of different maceration times (0, 2, 4, 8 and 14 days) after pulsed electric field (PEF) processing (1.5 kV/cm, either at 15 or 70 kJ/kg) on the release of anthocyanins from Merlot grapes (Vitis vinifera) and the bioprotective potentials of grape juice against H2O2-induced oxidative stress using human intestinal Caco-2 cell culture model. Cell viability, lactate dehydrogenase membrane leakage and nitric oxide production in Caco-2 cells were used as biomarkers to indicate general cellular health and integrity that ultimately represent the bioprotective potentials of grape juice. The results showed that PEF at 70 kJ/kg was the most effective in accelerating the release of anthocyanins from grape skin. Furthermore, the amount and the type of anthocyanins being released varied as a result of combined effect of PEF processing intensity and maceration time. Linear correlations between anthocyanins and the bioprotective capacity markers (R 2 = 0.4–0.8) were found. Compared to the untreated Merlot, PEF treatment either at 15 or 70 kJ/kg reduced the maceration time from 14 to 8 and 2 days, respectively, to achieve similar degree of bioprotective effect. This implies the possibility of using combined PEF and maceration time to tailor the profile of bioactive compounds with the same bioprotective potentials.
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References
Ainsworth, E. A., & Gillespie, K. M. (2007). Estimation of total phenolic content and other oxidation substrates in plant tissues using folin-ciocalteu reagent. Nature Protocols, 2(4), 875–877.
Apel, K., & Hirt, H. (2004). Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 55(1), 373–399.
Berridge, M. V., & Tan, A. S. (1993). Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): Subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Archives of Biochemistry and Biophysics, 303(2), 474–482.
Bobinaitė, R., Pataro, G., Lamanauskas, N., Šatkauskas, S., Viškelis, P., & Ferrari, G. (2015). Application of pulsed electric field in the production of juice and extraction of bioactive compounds from blueberry fruits and their by-products. Journal of Food Science and Technology, 52(9), 5898–5905.
Boussetta, N., Lebovka, N., Vorobiev, E. N., Adenier, H., Bedel-Cloutour, C., & Lanoisellé, J.-L. (2009). Electrically assisted extraction of soluble matter from Chardonnay grape skins for polyphenol recovery. Journal of Agricultural and Food Chemistry, 57(4), 1491–1497.
Burney, S., Caulfield, J. L., Niles, J. C., Wishnok, J. S., & Tannenbaum, S. R. (1999). The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutation Research, Fundamental and Molecular Mechanisms of Mutagenesis, 424(1–2), 37–49.
Chacón, M. R., Ceperuelo-Mallafré, V., Maymó-Masip, E., Mateo-Sanz, J. M., Arola, L., Guitiérrez, C., et al. (2009). Grape-seed procyanidins modulate inflammation on human differentiated adipocytes in vitro. Cytokine, 47(2), 137–142.
Chaovanalikit, A., & Wrolstad, R. E. (2004). Anthocyanin and polyphenolic composition of fresh and processed cherries. Journal of Food Science, 69(1), FCT73–FCT83.
Cholet, C., Delsart, C., Petrel, M., Gontier, E., Grimi, N., L’Hyvernay, A., et al. (2014). Structural and biochemical changes induced by pulsed electric field treatments on Cabernet Sauvignon grape berry skins: Impact on cell wall total tannins and polysaccharides. Journal of Agricultural and Food Chemistry, 62(13), 2925–2934.
Corrales, M., Toepfl, S., Butz, P., Knorr, D., & Tauscher, B. (2008). Extraction of anthocyanins from grape by-products assisted by ultrasonics, high hydrostatic pressure or pulsed electric fields: a comparison. Innovative Food Science & Emerging Technologies, 9(1), 85–91.
Delsart, C., Cholet, C., Ghidossi, R., Grimi, N., Gontier, E., Gény, L., et al. (2013). Effects of pulsed electric fields on Cabernet Sauvignon grape berries and on the characteristics of wines. Food and Bioprocess Technology, 1–13.
Delsart, C., Ghidossi, R., Poupot, C., Cholet, C., Grimi, N., Vorobiev, E., et al. (2012). Enhanced extraction of phenolic compounds from Merlot grapes by pulsed electric field. American Journal of Enology and Viticulture, 63(2), 205–211.
Dimitrovska, M., Bocevska, M., Dimitrovski, D., & Murkovic, M. (2011). Anthocyanin composition of Vranec, Cabernet Sauvignon, Merlot and Pinot Noir grapes as indicator of their varietal differentiation. European Food Research and Technology, 232(4), 591–600.
Donsì, F., Ferrari, G., Fruilo, M., & Pataro, G. (2010a). Pulsed electric field-assisted vinification of Aglianico and Piedirosso grapes. Journal of Agricultural and Food Chemistry, 58(22), 11606–11615.
Donsì, F., Ferrari, G., & Pataro, G. (2010b). Applications of pulsed electric field treatments for the enhancement of mass transfer from vegetable tissue. Food Engineering Reviews, 2(2), 109–130.
El Darra, N., Grimi, N., Vorobiev, E., Louka, N., & Maroun, R. (2013a). Extraction of polyphenols from red grape pomace assisted by pulsed ohmic heating. Food and Bioprocess Technology, 6(5), 1281–1289.
El Darra, N., Grimi, N., Vorobiev, E., Maroun, R. G., & Louka, N. (2013b). Pulsed electric field-assisted cold maceration of Cabernet Franc and Cabernet Sauvignon grapes. American Journal of Enology and Viticulture, 64(4), 476–484.
Ghosh, D., McGhie, T. K., Zhang, J., Adaim, A., & Skinner, M. (2006). Effects of anthocyanins and other phenolics of boysenberry and blackcurrant as inhibitors of oxidative stress and damage to cellular DNA in SH-SY5Y and HL-60 cells. Journal of the Science of Food and Agriculture, 86(5), 678–686.
Glahn, R. P., Lai, C., Hsu, J., Thompson, J. F., Guo, M. R., & Van Campen, D. R. (1998). Decreased citrate improves iron availability from infant formula: Application of an in vitro digestion/Caco-2 cell culture model. The Journal of Nutrition, 128(2), 257–264.
Glories, Y. (1984). La coleur des vins rouges: 1° partie “les equilibres des anthocyanes et des tanins. Connaisance Vigne Vin, 18, 195–217.
Gómez-Plaza, E., Miñano, A., & López-Roca, J. M. (2006). Comparison of chromatic properties, stability and antioxidant capacity of anthocyanin-based aqueous extracts from grape pomace obtained from different vinification methods. Food Chemistry, 97(1), 87–94.
Grimi, N., Dubois, A., Marchal, L., Jubeau, S., Lebovka, N. I., & Vorobiev, E. (2014). Selective extraction from microalgae Nannochloropsis sp. using different methods of cell disruption. Bioresource Technology, 153(0), 254–259.
Grimi, N., Lebovka, N. I., Vorobiev, E., & Vaxelaire, J. (2009). Effect of a pulsed electric field treatment on expression behavior and juice quality of Chardonnay grape. Food Biophysics, 4(3), 191–198.
Heo, H. J., & Lee, C. Y. (2005). Strawberry and its anthocyanins reduce oxidative stress-induced apoptosis in PC12 cells. Journal of Agricultural and Food Chemistry, 53(6), 1984–1989.
Heredia, F. J., Escudero-Gilete, M. L., Hernanz, D., Gordillo, B., Meléndez-Martínez, A. J., Vicario, I. M., et al. (2010). Influence of the refrigeration technique on the colour and phenolic composition of Syrah red wines obtained by pre-fermentative cold maceration. Food Chemistry, 118(2), 377–383.
Leong, S. Y., & Oey, I. (2012). Effects of processing on anthocyanins, carotenoids and vitamin C in summer fruits and vegetables. Food Chemistry, 133(4), 1577–1587.
Liu, D., Lebovka, N. I., & Vorobiev, E. (2013). Impact of electric pulse treatment on selective extraction of intracellular compounds from Saccharomyces cerevisiae yeasts. Food and Bioprocess Technology, 6(2), 576–584.
López, N., Puértolas, E., Hernández-Orte, P., Álvarez, I., & Raso, J. (2009). Effect of a pulsed electric field treatment on the anthocyanins composition and other quality parameters of Cabernet Sauvignon freshly fermented model wines obtained after different maceration times. LWT - Food Science and Technology, 42(7), 1225–1231.
Luengo, E., Franco, E., Ballesteros, F., Álvarez, I., & Raso, J. (2014). Winery trial on application of pulsed electric fields for improving vinification of Garnacha grapes. Food and Bioprocess Technology, 7(5), 1457–1464.
Miranda-Rottmann, S., Aspillaga, A. A., Pérez, D. D., Vasquez, L., Martinez, A. L. F., & Leighton, F. (2002). Juice and phenolic fractions of the berry Aristotelia chilensis inhibit LDL oxidation in vitro and protect human endothelial cells against oxidative stress. Journal of Agricultural and Food Chemistry, 50(26), 7542–7547.
Moskowitz, A. H., & Hrazdina, G. (1981). Vacuolar contents of fruit subepidermal cells from Vitis species. Plant Physiology, 68(3), 686–692.
Ortega-Regules, A., Ros-García, J. M., Bautista-Ortín, A. B., López-Roca, J. M., & Gómez-Plaza, E. (2008). Differences in morphology and composition of skin and pulp cell walls from grapes (Vitis vinifera L.): Technological implications. European Food Research and Technology, 227(1), 223–231.
Parniakov, O., Lebovka, N. I., Hecke, E., & Vorobiev, E. (2014). Pulsed electric field assisted pressure extraction and solvent extraction from mushroom (Agaricus bisporus). Food and Bioprocess Technology, 7(1), 174–183.
Pinelo, M., Arnous, A., & Meyer, A. S. (2006). Upgrading of grape skins: Significance of plant cell-wall structural components and extraction techniques for phenol release. Trends in Food Science and Technology, 17(11), 579–590.
Praporscic, I., Lebovka, N. I., Vorobiev, E., & Mietton-Peuchot, M. (2007). Pulsed electric field enhanced expression and juice quality of white grapes. Separation and Purification Technology, 52(3), 520–526.
Puértolas, E., López, N., Condón, S., Álvarez, I., & Raso, J. (2010a). Potential applications of PEF to improve red wine quality. Trends in Food Science and Technology, 21(5), 247–255.
Puértolas, E., Saldaña, G., Álvarez, I., & Raso, J. (2011). Experimental design approach for the evaluation of anthocyanin content of rosé wines obtained by pulsed electric fields: Influence of temperature and time of maceration. Food Chemistry, 126(3), 1482–1487.
Puértolas, E., Saldaña, G., Condón, S., Álvarez, I., & Raso, J. (2010b). Evolution of polyphenolic compounds in red wine from Cabernet Sauvignon grapes processed by pulsed electric fields during aging in bottle. Food Chemistry, 119(3), 1063–1070.
Racher, A. J., Looby, D., & Griffiths, J. B. (1990). Use of lactate dehydrogenase release to assess changes in culture viability. Cytotechnology, 3(3), 301–307.
Ramón Martı́n, A., Villegas, I., La Casa, C., & de la Lastra, C. A. (2004). Resveratrol, a polyphenol found in grapes, suppresses oxidative damage and stimulates apoptosis during early colonic inflammation in rats. Biochemical Pharmacology, 67(7), 1399–1410.
Redondo, L.M., Andrade, J., Santos, J.O., Barros, F., & Pereira, M.T. (2012). Industrial processing of red and white grapes assisted by pulsed electric fields. In 4th Euro-Asian Pulsed Power Conference and the 19th International Conference on High-Power Particle Beams, Karlsruhe, Germany, September 30 - October 4 2012.
Romero-Cascales, I., Ortega-Regules, A., López-Roca, J. M., Fernández-Fernández, J. I., & Gómez-Plaza, E. (2005). Differences in anthocyanin extractability from grapes to wines according to variety. American Journal of Enology and Viticulture, 56(3), 212–219.
Sacchi, K. L., Bisson, L. F., & Adams, D. O. (2005). A review of the effect of winemaking techniques on phenolic extraction in red wines. American Journal of Enology and Viticulture, 56(3), 197–206.
Shih, P.-H., Yeh, C.-T., & Yen, G.-C. (2007). Anthocyanins induce the activation of phase II enzymes through the antioxidant response element pathway against oxidative stress-induced apoptosis. Journal of Agricultural and Food Chemistry, 55(23), 9427–9435.
Spencer, J. P. E., Abd El Mohsen, M. M., & Rice-Evans, C. (2004). Cellular uptake and metabolism of flavonoids and their metabolites: Implications for their bioactivity. Archives of Biochemistry and Biophysics, 423(1), 148–161.
Wang, J., & Mazza, G. (2002). Inhibitory effects of anthocyanins and other phenolic compounds on nitric oxide production in LPS/IFN-γ-activated RAW 264.7 macrophages. Journal of Agricultural and Food Chemistry, 50(4), 850–857.
Youdim, K. A., Martin, A., & Joseph, J. A. (2000). Incorporation of the elderberry anthocyanins by endothelial cells increases protection against oxidative stress. Free Radical Biology and Medicine, 29(1), 51–60.
Zhang, B., Kang, M., Xie, Q., Xu, B., Sun, C., Chen, K., et al. (2010). Anthocyanins from Chinese bayberry extract protect β cells from oxidative stress-mediated injury via HO-1 upregulation. Journal of Agricultural and Food Chemistry, 59(2), 537–545.
Zhang, Q. H., Barbosa-Cánovas, G. V., & Swanson, B. G. (1995). Engineering aspects of pulsed electric field pasteurization. Journal of Food Engineering, 25(2), 261–281.
Zimmermann, U., Pilwat, G., Beckers, F., & Riemann, F. (1976). Effects of external electrical fields on cell membranes. Bioelectrochemistry and Bioenergetics, 3(1), 58–83.
Acknowledgments
The research was funded by University of Otago Priming Partnership funding. The authors thank Villa Maria Estates winery for their in-kind provision of grapes throughout the study. SY Leong acknowledges University of Otago (UO) Doctoral Scholarship towards her PhD study. We also thank Vidya Kethireddy, Nerida Downes, Ian Ross, Sarah Henry, Jo’ann Ayers and Pui Yee Lee (Food Science, UO), Ian Stewart and Jenny Lyburn (Chemistry, UO) for their technical assistance.
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Leong, S.Y., Burritt, D.J. & Oey, I. Effect of Combining Pulsed Electric Fields with Maceration Time on Merlot Grapes in Protecting Caco-2 Cells from Oxidative Stress. Food Bioprocess Technol 9, 147–160 (2016). https://doi.org/10.1007/s11947-015-1604-y
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DOI: https://doi.org/10.1007/s11947-015-1604-y