Consumption of Oriental Plums Improved the Cognitive Performance and Modulated the Cerebral Neurodegeneration-Related Protein Expressions in Rats with Nicotinamide/Streptozotocin-Induced Diabetes

DOI: 10.4236/fns.2013.411148   PDF   HTML     3,465 Downloads   5,018 Views   Citations

Abstract

To examine the effect of consuming polyphenol-rich Oriental plum (Prunus salicina Lindl) on the cognitive performance and the expressions of cerebral neurodegeneration-related proteins in diabetic rats, Wistar rats were assigned into 4 groups: control (C, n = 14), nicotinamide/streptozotocin-induced DM rats (DM, n = 13), DM rats fed metformin (0.05% w/w in the diet, MT, n = 18), and DM rats fed freeze-dried oriental plum powder (2% w/w in the diet, OP, n = 16) for 2 months. The cognitive performance was evaluated by testing in a Morris water maze. The insulin resistance, serum lipid peroxidation, expressions of pathological proteins of AD, beta-amyloid (Aβ) and phosphorylated tau protein were also measured. Consumption of plums significantly improved the spatial learning ability, reduced the insulin resistance, lipid peroxidation, Aβ and phosphorylated tau protein expressions in the cerebral cortex (all P < 0.05), and decreased Aβ deposition in the hippocampus of diabetic rats. In conclusion, polyphenol-rich Oriental plums ameliorated the cognitive decline and reduced the expressions of pathological proteins of AD by possibly reducing hyperglycemia, insulin resistance, and oxidative stress in diabetic rats.

Share and Cite:

K. Lee, Y. Chen, C. Lin, W. Chiu, H. Liao and S. Lin, "Consumption of Oriental Plums Improved the Cognitive Performance and Modulated the Cerebral Neurodegeneration-Related Protein Expressions in Rats with Nicotinamide/Streptozotocin-Induced Diabetes," Food and Nutrition Sciences, Vol. 4 No. 11, 2013, pp. 1145-1154. doi: 10.4236/fns.2013.411148.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] S. A. Park, “A Common Pathogenic Mechanism Linking Type-2 Diabetes and Alzheimer’s Disease: Evidence from Animal Models,” Journal of Clinical Neurology, Vol. 7, No. 1, 2011, pp. 10-18.
http://dx.doi.org/10.3988/jcn.2011.7.1.10
[2] S. C. Correia, R. X. Santos, G. Perry, X. Zhu, P. I. Moreira and M. A. Smith, “Insulin-Resistant Brain State: The Culprit in Sporadic Alzheimer’s Disease?” Ageing Research Reviews, Vol. 10, No. 2, 2011, pp. 264-273. http://dx.doi.org/10.1016/j.arr.2011.01.001
[3] H. W. Querfurth and F. M. LaFerla, “Alzheimer’s Disease,” New England Journal of Medicine, Vol. 362, 2010, pp. 329-344. http://dx.doi.org/10.1056/NEJMra0909142
[4] D. Hirtz, D. J. Thurman, K. Gwinn-Hardy, M. Mohamed, A. R. Chaudhuri and R. Zalutsky, “How Common Are the ‘Common’ Neurologic Disorders?” Neurology, Vol. 68, No. 5, 2007, pp. 326-337.
http://dx.doi.org/10.1212/01.wnl.0000252807.38124.a3
[5] A. Rocchi, S. Pellegrini, G. Siciliano and L. Murri, “Cau sative and Susceptibility Genes for Alzheimer’s Disease: A Review,” Brain Research Bulletin, Vol. 61, No. 1, 2003, pp. 1-24.
http://dx.doi.org/10.1016/S0361-9230(03)00067-4
[6] J. Janson, T. Laedtke, J. E. Parisi, P. O’Brien, R. C. Pe tersen and P. C. Butler, “Increased Risk of Type 2 Diabe tes in Alzheimer Disease,” Diabetes, Vol. 53, No. 2, 2004, pp. 474-481.
http://dx.doi.org/10.2337/diabetes.53.2.474
[7] B. Kim, C. Backus, S. Oh, J. M. Hayes and E. L. Feldman, “Increased Tau Phosphorylation and Cleavage in Mouse Models of Type 1 and Type 2 Diabetes,” Endocrinology, Vol. 150, No. 12, 2009, pp. 5294-5301. http://dx.doi.org/10.1210/en.2009-0695
[8] A. Gupta, B. Bisht and C. S. Dey, “Peripheral Insulin Sensitizer Drug Metformin Ameliorates Neuronal Insulin Resistance and Alzheimer’s-Like Changes,” Neurophar macology, Vol. 60, No. 6, 2011, pp. 910-920. http://dx.doi.org/10.1016/j.neuropharm.2011.01.033
[9] E. C. McNay and A. K. Recknagel, “Brain Insulin Sig naling: A Key Component of Cognitive Processes and a Potential Basis for Cognitive Impairment in Type 2 Diabetes,” Neurobiology of Learning and Memory, Vol. 96, No. 3, 2011, pp. 432-442. http://dx.doi.org/10.1016/j.nlm.2011.08.005
[10] A. Scalbert, C. Manach, C. Morand, C. Remesy and L. Jimenez, “Dietary Polyphenols and the Prevention of Dis eases,” Critical Reviews in Food Science and Nutrition, Vol. 45, No. 4, 2005, pp. 287-306. http://dx.doi.org/10.1080/1040869059096
[11] R. J. Williams and J. P. Spencer, “Flavonoids, Cognition, and Dementia: Actions, Mechanisms, and Potential Ther apeutic Utility for Alzheimer Disease,” Free Radical Biology and Medicine, Vol. 52, No. 1, 2012, pp. 35-45. http://dx.doi.org/10.1016/j.freeradbiomed.2011.09.010
[12] J. P. Pencer, “The Impact of Fruit Flavonoids on Memory and Cognition,” British Journal of Nutrition, Vol. 104, Suppl. 3, 2010, pp. S40-S47. http://dx.doi.org/10.1017/S0007114510003934
[13] R. Krikorian, M. D. Shidler, T. A. Nash, W. Kalt, M. R. Vinqvist-Tymchuk, B. Shukitt-Hale and J. A. Joseph, “Blueberry Supplementation Improves Memory in Older Adults,” Journal of Agricultural and Food Chemistry, Vol. 58, No. 7, 2010, pp. 3996-4000. http://dx.doi.org/10.1021/jf9029332
[14] F. C. Lau, B. Shukitt-Hale and J. A. Joseph, “The Benefi cial Effects of Fruit Polyphenols on Brain Aging,” Neurobiol Aging, Vol. 26, Suppl. 1, 2005, pp. 128-132.
http://dx.doi.org/10.1016/j.neurobiolaging.2005.08.007
[15] D.-O. Kim, O. K. Chun, Y. J. Kim, H.-Y. Moon and C. Y. Lee, “Quantification of Polyphenolics and Their Antioxi dant Capacity in Fresh Plums,” Journal of Agricultural and Food Chemistry, Vol. 51, No. 22, 2003, pp. 6509-6515. http://dx.doi.org/10.1021/jf0343074
[16] B. Shukitt-Hale, W. Kalt, A. N. Carey, M. Vinqvist Tymchuk, J. McDonald and J. A. Joseph, “Plum Juice, but Not Dried Plum Powder, Is Effective in Mitigating Cognitive Deficits in Aged Rats,” Nutrition, Vol. 25, No. 5, 2009, pp. 567-573. http://dx.doi.org/10.1016/j.nut.2008.10.018
[17] B. Shukitt-Hale, V. Cheng and J. A. Joseph, “Effects of Blackberries on Motor and Cognitive Function in Aged Rats,” Nutritional Neuroscience, Vol. 12, No. 3, 2009, pp. 135-140.
http://dx.doi.org/10.1179/147683009X423292
[18] Y. Tanaka, H. Uchino, T. Shimizu, H. Yoshii, M. Niwa, C. Ohmura, N. Mitsuhashi, T. Onuma and R. Kawamori, “Effect of Metformin on Advanced Glycation Endproduct Formation and Peripheral Nerve Function in Streptozoto cin-Induced Diabetic Rats,” European Journal of Phar macology, Vol. 376, No. 1-2, 1999, pp. 17-22. http://dx.doi.org/10.1016/S0014-2999(99)00342-8
[19] D.-O. Kim and C. Lee, “Extraction and Isolation of Poly phenolics,” Current Protocols in Food Analytical Chem istry, Vol. 6, 2003, pp. I1.2.1-I1.2.12.
[20] E. A. Ainsworth and K. M. Gillespie, “Estimation of Total Phenolic Content and Other Oxidation Substrates in Plant Tissues Using Folin-Ciocalteu Reagent,” Nature Protocols, Vol. 2, 2007, pp. 875-877. http://dx.doi.org/10.1038/nprot.2007.102
[21] M. M. Giusti and R. E. Wrolstad, “Characterization and Measurement of Anthocyanins by UV-Visible Spectros copy in Current Protocols in Food Analytical Chemistry,” John Wiley & Sons, Inc., 2001.
[22] C. W. Chen and H. H. Cheng, “A Rice Bran Oil Diet Increases LDL-Receptor and HMG-CoA Reductase mRNA Expressions and Insulin Sensitivity in Rats with Strepto zotocin/Nicotinamide-Induced Type 2 Diabetes,” Journal of Nutrition, Vol. 136, 2006, pp. 1472-1476.
[23] D. R. Matthews, J. P. Hosker, A. S. Rudenski, B. A. Nay lor, D. F. Treacher and R. C. Turner, “Homeostasis Model Assessment: Insulin Resistance and Beta-Cell Function from Fasting Plasma Glucose and Insulin Concentrations in Man,” Diabetologia, Vol. 28, No. 7, 1985, pp. 412-419.
http://dx.doi.org/10.1007/BF00280883
[24] K. Yagi, “Simple Assay for the Level of Total Lipid Peroxides in Serum or Plasma,” Methods in Molecular Biology, Vol. 108, 1998, pp. 101-106.
[25] C. V. Vorhees and M. T. Williams, “Morris Water Maze: Procedures for Assessing Spatial and Related Forms of Learning and Memory,” Nature Protocols, Vol. 1, 2006, pp. 848-858.
http://dx.doi.org/10.1038/nprot.2006.116
[26] L. Escribano, A. M. Simon, E. Gimeno, M. Cuadrado Tejedor, R. Lopez de Maturana, A. Garcia-Osta, A. Ri cobaraza, A. Perez-Mediavilla, J. Del Rio and D. Fre chilla, “Rosiglitazone Rescues Memory Impairment in Alzheimer’s Transgenic Mice: Mechanisms Involving a Reduced Amyloid and Tau Pathology,” Neuropsycho pharmacology, Vol. 35, 2010, pp. 1593-1604.
http://dx.doi.org/10.1038/npp.2010.32
[27] P. Masiello, C. Broca, R. Gross, M. Roye, M. Manteg hetti, D. Hillaire-Buys, M. Novelli and G. Ribes, “Expe rimental NIDDM: Development of a New Model in Adult Rats Administered Streptozotocin and Nicotinamide,” Diabetes, Vol. 47, No. 2, 1998, pp. 224-229. http://dx.doi.org/10.2337/diab.47.2.224
[28] A. Griesmacher, M. Kindhauser, S. E. Andert, W. Sch reiner, C. Toma, P. Knoebl, P. Pietschmann, R. Prager, C. Schnack, G. Schernthaner, et al., “Enhanced Serum Levels of Thiobarbituric-Acid-Reactive Substances in Diabetes Mellitus,” American Journal of Medicine, Vol. 98, No. 5, 1995, pp. 469-475. http://dx.doi.org/10.1016/S0002-9343(99)80347-7
[29] T. Tsuda, F. Horio and T. Osawa, “Dietary Cyanidin 3-O Beta-D-Glucoside Increases ex Vivo Oxidation Resis tance of Serum in Rats,” Lipids, Vol. 33, No. 6, 1998, pp. 583-588.
http://dx.doi.org/10.1007/s11745-998-0243-5
[30] A. R. Collins, “Assays for Oxidative Stress and Antioxidant Status: Applications to Research into the Biological Effectiveness of Polyphenols,” American Journal of Cli nical Nutrition, Vol. 81, No. 1, 2005, pp. 261S-267S.
[31] V. Chauhan and A. Chauhan, “Oxidative Stress in Alzheimer’s Disease,” Pathophysiology, Vol. 13, No. 3, 2006, pp. 195-208. http://dx.doi.org/10.1016/j.pathophys.2006.05.004
[32] V. Kucukatay, A. Agar, S. Gumuslu and P. Yargicoglu, “Effect of Sulfur Dioxide on Active and Passive Avoid ance in Experimental Diabetes Mellitus: Relation to Oxi dant Stress and Antioxidant Enzymes,” International Journal of Neuroscience, Vol. 117, No. 8, 2007, pp. 1091-1107.
http://dx.doi.org/10.1080/00207450600934531
[33] G. J. Biessels, A. Kamal, G. M. Ramakers, I. J. Urban, B. M. Spruijt, D. W. Erkelens and W. H. Gispen, “Place Learning and Hippocampal Synaptic Plasticity in Streptozotocin-Induced Diabetic Rats,” Diabetes, Vol. 45, No. 9, 1996, pp. 1259-1266. http://dx.doi.org/10.2337/diab.45.9.1259
[34] A. Kamal, G. J. Biessels, I. J. Urban and W. H. Gispen, “Hippocampal Synaptic Plasticity in Streptozotocin-Dia betic Rats: Impairment of Long-Term Potentiation and Facilitation of Long-Term Depression,” Neuroscience, Vol. 90, No. 3, 1999, pp. 737-745. http://dx.doi.org/10.1016/S0306-4522(98)00485-0
[35] C. G. Jolivalt, C. A. Lee, K. K. Beiswenger, J. L. Smith, M. Orlov, M. A. Torrance and E. Masliah, “Defective In sulin Signaling Pathway and Increased Glycogen Synthase Kinase-3 Activity in the Brain of Diabetic Mice: Parallels with Alzheimer’s Disease and Correction by In sulin,” Journal of Neuroscience Research, Vol. 86, No. 15, 2008, pp. 3265-3274. http://dx.doi.org/10.1002/jnr.21787
[36] A. F. Schuh, C. M. Rieder, L. Rizzi, M. Chaves and M. Roriz-Cruz, “Mechanisms of Brain Aging Regulation by Insulin: Implications for Neurodegeneration in Late-On set Alzheimer’s Disease,” ISRN Neurology, Vol. 2011, 2011, Article ID: 306905.
[37] K. Maiese, S. D. Morhan and Z. Z. Chong, “Oxidative Stress Biology and Cell Injury during Type 1 and Type 2 Diabetes Mellitus,” Current Neurovascular Research, Vol. 4, No. 1, 2007, pp. 63-71. http://dx.doi.org/10.2174/156720207779940653

  
comments powered by Disqus

Copyright © 2020 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.