Effect of Italian Sour Cherry (Prunus cerasus L.) on the Formation of Advanced Glycation End Products and Lipid Peroxidation

Gianna Ferretti, Davide Neri, Tiziana Bacchetti

Dipartimento d Scienze Cliniche Sperimentali e Odontostomatologiche, Università Politecnica delle Marche, Ancona, Italy.
Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche, Ancona, Italy.
SAPROV—Dipartimento di Scienze Ambientali e delle Produzioni Vegetali, Università Politecnica delle Marche, Ancona, Italy.

DOI: 10.4236/fns.2014.516170                

Abstract

Sweet and sour cherries contain several polyphenols that possess antioxidant and anti-inflammatory properties. Aim of this study was to investigate the effect of the maturity stage on phenol content and biological properties of extract of a local Morello-type of sour cherry (Prunus cerasus L.), “visciola”. The study of total phenol content and total antioxidant potential was associated with the evaluation of the antioxidant property of extracts using a copper catalyzed human low density lipoproteins (LDL) oxidation as experimental model. Moreover, using albumin glycated by methylglyoxal, we evaluated the anti-glycation effect of fruit extract. The results demonstrated that fully ripened fruits exert higher antioxidant and anti-glycation properties when compared with partially ripened fruits. Information about the health-promoting components of “visciola” could lead to a better understanding and an increased consumption of these, including its use as functional food.

Keywords

Sour Cherry, “Visciola”, Antioxidants, Fruit Maturation, LDL Oxidation, Glycation, Methylglyoxal, Advanced Glycation End Products, Polyphenols

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Kris-Etherton, P.M., Hecker, K.D., Bonanome, A., Coval, S.M., Binkoski, A.E. and Hilpert, K.F. (2002) Bioactive Compounds in Foods: Their Role in the Prevention of Cardiovascular Disease and Cancer. The American Journal of Medicine, 113, 71S-88S. http://dx.doi.org/10.1016/S0002-9343(01)00995-0
[2]	Tangney, C.C. and Rasmussen, H.E. (2013) Polyphenols, Inflammation, and Cardiovascular Disease. Current Atherosclerosis Reports, 15, 324. http://dx.doi.org/10.1007/s11883-013-0324-x
[3]	Babu, P.V.A., Liu, D.M. and Gilbert, E.R. (2013) Recent Advances in Understanding the Anti-Diabetic Actions of Dietary Flavonoids. Journal of Nutritional Biochemistry, 24, 1777-1789. http://dx.doi.org/10.1016/j.jnutbio.2013.06.003
[4]	Williamson, G. (2013) Possible Effects of Dietary Polyphenols on Sugar Absorption and Digestion. Molecular Nutrition & Food Research, 57, 48-57. http://dx.doi.org/10.1002/mnfr.201200511
[5]	Jariyapamornkoon, N., Yibchok-anun, S. and Adisakwattana, S. (2013) Inhibition of Advanced Glycation End Products by Red Grape Skin Extract and Its Antioxidant Activity. BMC Complementary and Alternative Medicine, 13, 171. http://dx.doi.org/10.1186/1472-6882-13-171
[6]	Lavelli, V. (2009) Combined Effect of Storage Temperature and Water Activity on the Antiglycoxidative Properties and Color of Dehydrated Apples. Journal of Agricultural and Food Chemistry, 57, 11491-11497. http://dx.doi.org/10.1021/jf901865r
[7]	Matsuda, H., Wang, T., Managi, H. and Yoshikawa, M. (2003) Structural Requirements of Flavonoids for Inhibition of Protein Glycation and Radical Scavenging Activities. Bioorganic & Medicinal Chemistry, 11, 5317-5323. http://dx.doi.org/10.1016/j.bmc.2003.09.045
[8]	Peng, X., Ma, J., Chen, F. and Wang, M. (2011) Naturally Occurring Inhibitors against the Formation of Advanced Glycation End-Products. Food & Function, 2, 289-301. http://dx.doi.org/10.1039/c1fo10034c
[9]	Shao, X., Bai, N.S., He, K., Ho, C.T., Yang, C.S. and Sang, S.M. (2008) Apple Polyphenols, Phloretin and Phloridzin: New Trapping Agents of Reactive Dicarbonyl Species. Chemical Research in Toxicology, 21, 2042-2050. http://dx.doi.org/10.1021/tx800227v
[10]	Wu, C.H., Huang, S.M., Lin, J.A. and Yen, G.C. (2011) Inhibition of Advanced Glycation Endproduct Formation by Foodstuffs. Food & Function, 2, 224-234. http://dx.doi.org/10.1039/c1fo10026b
[11]	Ahmed, N. (2005) Advanced Glycation Endproducts—Role in Pathology of Diabetic Complications. Diabetes Research and Clinical Practice, 67, 3-21. http://dx.doi.org/10.1016/j.diabres.2004.09.004
[12]	Srikanth, V., Maczurek, A., Phan, T., Steele, M., Westcott, B., Juskiw, D. and Münch, G. (2011) Advanced Glycation Endproducts and Their Receptor RAGE in Alzheimer’s Disease. Neurobiology of Aging, 32, 763-777. http://dx.doi.org/10.1016/j.neurobiolaging.2009.04.016
[13]	Thornalley, P.J. (1996) Pharmacology of Methylglyoxal: Formation, Modification of Proteins and Nucleic Acids, and Enzymatic Detoxification—A Role in Pathogenesis and Antiproliferative Chemotherapy. General Pharmacology, 27, 565-573. http://dx.doi.org/10.1016/0306-3623(95)02054-3
[14]	Wolff, S.P. and Dean, R.T. (1987) Glucose Autoxidation and Protein Modification. The Potential Role of “Autoxidative Glycosylation” in Diabetes. Biochemical Journal, 245, 243-250.
[15]	Ames, B.N., Shigenaga, M.K. and Hagen, T.M. (1993) Oxidants, Antioxidants, and the Degenerative Diseases of Aging. Proceedings of the National Academy of Sciences of the United States of America, 90, 7915-7922. http://dx.doi.org/10.1073/pnas.90.17.7915
[16]	Meydani, M. (2002) The Boyd Orr Lecture: Nutrition Interventions in Aging and Age-Associated Disease. Proceedings of the Nutrition Society, 61, 165-171. http://dx.doi.org/10.1079/PNS2002144
[17]	Chaovanalikit, A. and Wrolstad, R.E. (2004) Total Anthocyanins and Total Phenolics of Fresh and Processed Cherries and Their Antioxidant Properties. Journal of Food Science, 69, FCT67-FCT72. http://dx.doi.org/10.1111/j.1365-2621.2004.tb17858.x
[18]	Ferretti, G., Bacchetti, T., Belleggia, A. and Neri, D. (2010) Cherry Antioxidants: From Farm to Table. Molecules, 15, 6993-7005. http://dx.doi.org/10.3390/molecules15106993
[19]	Goncalves, B., Landbo, A.K., Knudsen, D., Silva, A.P., Moutinho-Pereira, J., Rosa, E. and Meyer, A.S. (2004) Effect of Ripeness and Postharvest Storage on the Phenolic Profiles of Cherries (Prunus avium L.). Journal of Agricultural and Food Chemistry, 52, 523-530. http://dx.doi.org/10.1021/jf030595s
[20]	Kirakosyan, A., Seymour, E.M., Llanes, D.E.U., Kaufman, P.B. and Bolling, S.F. (2009) Chemical Profile and Antioxidant Capacities of Tart Cherry Products. Food Chemistry, 115, 20-25. http://dx.doi.org/10.1016/j.foodchem.2008.11.042
[21]	Heinonen, I.M., Meyer, A.S. and Frankel, E.N. (1998) Antioxidant Activity of Berry Phenolics on Human Low-Density Lipoprotein and Liposome Oxidation. Journal of Agricultural and Food Chemistry, 46, 4107-4112. http://dx.doi.org/10.1021/jf980181c
[22]	Ou, B.X., Bosak, K.N., Brickner, P.R., Iezzoni, D.G. and Seymour, E.M. (2012) Processed Tart Cherry Products- Comparative Phytochemical Content, in Vitro Antioxidant Capacity and in Vitro Anti-Inflammatory Activity. Journal of Food Science, 77, H105-H112. http://dx.doi.org/10.1111/j.1750-3841.2012.02681.x
[23]	Jacob, R.A., Spinozzi, G.M., Simon, V.A., Kelley, D.S., Prior, R.L., Hess-Pierce, B. and Kader, A.A. (2003) Consumption of Cherries Lowers Plasma Urate in Healthy Women. Journal of Nutrition, 133, 1826-1829.
[24]	Prior, R.L., Go, L.W., Wu, X.L., Jacob, R.A., Sotoudeh, G., Kader, A.A. and Cook, R.A. (2007) Plasma Antioxidant Capacity Changes Following a Meal as a Measure of the Ability of a Food to Alter in Vivo Antioxidant Status. Journal of the American College of Nutrition, 26, 170-181. http://dx.doi.org/10.1080/07315724.2007.10719599
[25]	Traustadottir, T., Davies, S.S., Stock, A.A., Su, Y., Heward, C.B., Roberts II, L.J. and Harman, S.M. (2009) Tart Cherry Juice Decreases Oxidative Stress in Healthy Older Men and Women. Journal of Nutrition, 139, 1896-1900. http://dx.doi.org/10.3945/jn.109.111716
[26]	Diaz-Mula, H.M., Castillo, S., Martinez-Romero, D., Valero, D., Zapata, P.J., Guillen, F. and Serrano, M. (2009) Sensory, Nutritive and Functional Properties of Sweet Cherry as Affected by Cultivar and Ripening Stage. Food Science and Technology International, 15, 535-543. http://dx.doi.org/10.1177/1082013209351868
[27]	Goldman, I.L., Kader, A.A. and Heintz, C. (1999) Influence of Production, Handling, and Storage on Phytonutrient Content of Foods. Nutrition Reviews, 57, S46-S52. http://dx.doi.org/10.1111/j.1753-4887.1999.tb01807.x
[28]	Singleton, V.L., Orthofer, R. and Lamuela-Raventos, R.M. (1999) Analysis of Total Phenols and Other Oxidation Substrates and Antioxidants by Means of Folin-Ciocalteu Reagent. Methods in Enzymology, 299, 152-178. http://dx.doi.org/10.1016/S0076-6879(99)99017-1
[29]	Gillespie, K.M., Chae, J.M. and Ainsworth, E.A. (2007) Rapid Measurement of Total Antioxidant Capacity in Plants. Nature Protocols, 2, 867-870. http://dx.doi.org/10.1038/nprot.2007.100
[30]	Cheng, Z., Moore, J. and Yu, L. (2006) High-Throughput Relative DPPH Radical Scavenging Capacity Assay. Journal of Agricultural and Food Chemistry, 54, 7429-7436. http://dx.doi.org/10.1021/jf0611668
[31]	Chung, B.H., Segrest, J.P., Ray, M.J., Brunzell, J.D., Hokanson, J.E., Krauss, R.M., Beaudrie, K. and Cone, J.T. (1986) Single Vertical Spin Density Gradient Ultracentrifugation. Methods in Enzymology, 128, 181-209. http://dx.doi.org/10.1016/0076-6879(86)28068-4
[32]	Bradford, M.M. (1976) A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Analytical Biochemistry, 72, 248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3
[33]	Esterbauer, H., Striegl, G., Puhl, H. and Rotheneder, M. (1989) Continuous Monitoring of in Vitro Oxidation of Human Low Density Lipoprotein. Free Radical Research, 6, 67-75. http://dx.doi.org/10.3109/10715768909073429
[34]	Gugliucci, A., Bastos, D.H., Schulze, J. and Souza, M.F. (2009) Caffeic and Chlorogenic Acids in Ilex paraguariensis Extracts Are the Main Inhibitors of AGE Generation by Methylglyoxal in Model Proteins. Fitoterapia, 80, 339-344. http://dx.doi.org/10.1016/j.fitote.2009.04.007
[35]	Lunceford, N. and Gugliucci, A. (2005) Ilex paraguariensis Extracts Inhibit AGE Formation More Efficiently than Green Tea. Fitoterapia, 76, 419-427. http://dx.doi.org/10.1016/j.fitote.2005.03.021
[36]	Goncalves, B., Landbo, A.K., Let, M., Silva, A.P., Rosa, E. and Meyer, A.S. (2004) Storage Affects the Phenolic Profiles and Antioxidant Activities of Cherries (Prunus avium L.) on Human Low-Density Lipoproteins. Journal of the Science of Food and Agriculture, 84, 1013-1020. http://dx.doi.org/10.1002/jsfa.1752
[37]	Serrano, M., Guillen, F., Martinez-Romero, D., Castillo, S. and Valero, D. (2005) Chemical Constituents and Antioxidant Activity of Sweet Cherry at Different Ripening Stages. Journal of Agricultural and Food Chemistry, 53, 2741-2745. http://dx.doi.org/10.1021/jf0479160
[38]	Serrano, M., Diaz-Mula, H.M., Zapata, P.J., Castillo, S., Guillen, F., Martinez-Romero, D., Valverde, J.M. and Valero, D. (2009) Maturity Stage at Harvest Determines the Fruit Quality and Antioxidant Potential after Storage of Sweet Cherry Cultivars. Journal of Agricultural and Food Chemistry, 57, 3240-3246. http://dx.doi.org/10.1021/jf803949k
[39]	Blando, F., Gerardi, C. and Nicoletti, I. (2004) Sour Cherry (Prunus cerasus L.) Anthocyanins as Ingredients for Functional Foods. Journal of Biomedicine and Biotechnology, 2004, 253-258. http://dx.doi.org/10.1155/S1110724304404136
[40]	Bonnefont-Rousselot, D. (2002) Glucose and Reactive Oxygen Species. Current Opinion in Clinical Nutrition & Metabolic Care, 5, 561-568. http://dx.doi.org/10.1097/00075197-200209000-00016
[41]	Bacchetti, T., Masciangelo, S., Armeni, T., Bicchiega, V. and Ferretti, G. (2014) Glycation of Human High Density Lipoprotein by Methylglyoxal: Effect on HDL-Paraoxonase Activity. Metabolism-Clinical and Experimental, 63, 307-311. http://dx.doi.org/10.1016/j.metabol.2013.10.013
[42]	Nagaraj, R.H., Oya-Ito, T., Padayatti, P.S., Kumar, R., Mehta, S., West, K., et al. (2003) Enhancement of Chaperone Function of Alpha-Crystallin by Methylglyoxal Modification. Biochemistry, 42, 10746-10755. http://dx.doi.org/10.1021/bi034541n
[43]	Shao, X., Chen, H., Zhu, Y., Sedighi, R., Ho, C.T. and Sang, S. (2014) Essential Structural Requirements and Additive Effects for Flavonoids to Scavenge Methylglyoxal. Journal of Agricultural and Food Chemistry, 62, 3202-3210. http://dx.doi.org/10.1021/jf500204s
[44]	Peng, X., Ma, J., Chao, J., Sun, Z., Chang, R.C., Tse, I., Li, E.T.S., Chen, F. and Wang, M.F. (2010) Beneficial Effects of Cinnamon Proanthocyanidins on the Formation of Specific Advanced Glycation Endproducts and Methylglyoxal- Induced Impairment on Glucose Consumption. Journal of Agricultural and Food Chemistry, 58, 6692-6696. http://dx.doi.org/10.1021/jf100538t
[45]	Fazzari, M., Fukumoto, L., Mazza, G., Livrea, M.A., Tesoriere, L. and Di Marco, L. (2008) In Vitro Bioavailability of Phenolic Compounds from Five Cultivars of Frozen Sweet Cherries (Prunus avium L.). Journal of Agricultural and Food Chemistry, 56, 3561-3568. http://dx.doi.org/10.1021/jf073506a
[46]	Manach, C., Scalbert, A., Morand, C., Remesy, C. and Jimenez, L. (2004) Polyphenols: Food Sources and Bioavailability. American Journal of Clinical Nutrition, 79, 727-747.