Journal of Food and Nutrition Research
ISSN (Print): 2333-1119 ISSN (Online): 2333-1240 Website: http://www.sciepub.com/journal/jfnr Editor-in-chief: Prabhat Kumar Mandal
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Journal of Food and Nutrition Research. 2014, 2(8), 450-456
DOI: 10.12691/jfnr-2-8-4
Open AccessArticle

Effects of Walnut Polyphenol on Learning and Memory Functions in Hypercholesterolemia Mice

Dandan Shi1, Chaoyin Chen1, , Shenglan Zhao2, Feng Ge1, Diqiu Liu1 and Hao Song1

1Faculty of life science, Kunming University of Science and Technology, Kunming, People's Republic of China

2Yunnan University of Traditional Chinese Medicine, Kunming, People's Republic of China

Pub. Date: July 31, 2014

Cite this paper:
Dandan Shi, Chaoyin Chen, Shenglan Zhao, Feng Ge, Diqiu Liu and Hao Song. Effects of Walnut Polyphenol on Learning and Memory Functions in Hypercholesterolemia Mice. Journal of Food and Nutrition Research. 2014; 2(8):450-456. doi: 10.12691/jfnr-2-8-4

Abstract

Evidence suggests that dietary walnuts are able to induce improvements in memory and learning functions. In addition, polyphenols have been shown to modulate critical neuronal signalling pathways involved in processes of learning and memory. The aim of our present work was to study the effect of polyphenol extracts from walnut testa (42%) on learning and memory functions in hypercholesterolemia mice based on obesity, hypercholesterolemia and oxidative stress. At the beginning of the experiment, mice were divided into 3 groups, one of them served as normol control group (NCG), the second as hypercholesterolemia control group (HCG), the last as walnut polyphenol-treated group (WTG). After 8 weeks of treatment, we investigated the performance of C57BL/6J mice in Morris water maze test. The results showed that the escape latency was significant increase in HCG, when compared to NCG and WTG. In addition, the number of crossings was significant decrease in HCG, when compared to NCG and WTG (–47.35% and –43.35%, respectively, P < 0.01). The swimming distance was longer in HCG than NCG and WTG [F (2,96) = 44.45, P < 0.001]. However, there was no significant difference in swimming speed among NCG, HCG and WTG [F (2, 96) = 0.167, P > 0.05]. On the other hand, walnut polyphenol (WP) significantly decreased serum total triglycerides, cholesterol and malondialdehyde (MDA) level (–36.31%, –31.48% and –21.51%, respectively, P < 0.01) and increased superoxide dismutase (SOD) activity (+48.39%, P < 0.01). Administration of WP significantly decreased MDA level (–36.86%, P < 0.01) and increased SOD activity (+17.08%, P < 0.01) in brain tissues. In conclusion, walnut polyphenol was able to improve learning and memory functions.

Keywords:
walnut polyphenol learning and memory functions obesity hypercholesterolemia oxidative stress

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

References:

[1]  Thompson, R.F., & Kim, J.J., Memory systems in the brain and localization of a memory. Proceedings of the national academy of sciences, 93 (24), 13438-13444, 1996.
 
[2]  Evola, M., Hall, A., Wall, T., Young, A., Grammas, P., Oxidative stress impairs learning and memory in apoE knockout mice. Pharmacology biochemistry and behavior, 96 (2), 181-186, 2010.
 
[3]  Moy G.A, McNay E.C., Caffeine prevents weight gain and cognitive impairment caused by a high-fat diet while elevating hippocampal BDNF. Physiology & behavior, 109: 69-74, 2013.
 
[4]  Farr, S.A., Yamada, K.A., Butterfield, D.A., Abdul, H.M., Xu, L., Miller, N.E., & Morley, J.E., Obesity and hypertriglyceridemia produce cognitive impairment. Endocrinology, 149 (5), 2628-2636, 2008.
 
[5]  Moreira, E.L.G., de Oliveira, J., Engel, D.F., Walz, R., de Bem, A.F., Farina, M., Prediger, R.D.S., Hypercholesterolemia induces short-term spatial memory impairments in mice: up-regulation of acetylcholinesterase activity as an early and causal event?. Journal of neural transmission, 1-12, 2013.
 
[6]  Solomon, A., Kivipelto, M., Wolozin, B., Zhou, J., Whitmer, R.A., Midlife serum cholesterol and increased risk of Alzheimer’s and vascular dementia three decades later. Dementia and geriatric cognitive disorders, 28 (1), 75-80, 2009.
 
[7]  Rea, T.D., Breitner, J.C., Psaty, B.M., Fitzpatrick, A.L., Lopez, O.L., Newman, A.B., Kuller, L.H., Statin use and the risk of incident dementia: the Cardiovascular Health Study. Archives of neurology, 62 (7), 1047-1051, 2005.
 
[8]  Ullrich, C., Pirchl, M., Humpel, C., Hypercholesterolemia in rats impairs the cholinergic system and leads to memory deficits. Molecular and cellular neuroscience, 45 (4), 408-417, 2010.
 
[9]  Evola, M., Hall, A., Wall, T., Young, A., & Grammas, P., Oxidative stress impairs learning and memory in apoE knockout mice. Pharmacology biochemistry and behavior, 96 (2), 181-186, 2010.
 
[10]  Ben Khaled, H., Ghlissi, Z., Chtourou, Y., Hakim, A., Ktari, N., Fatma, M. A., Nasri, M., Effect of protein hydrolysates from sardinelle (< i> Sardinella aurita</i>) on the oxidative status and blood lipid profile of cholesterol-fed rats. Food research international, 45 (1), 60-68, 2012.
 
[11]  Prasad K., Vitamin E and regression of hypercholesterolemia-induced oxidative stress in kidney. Molecular and cellular biochemistry, 385 (1-2): 17-21, 2014.
 
[12]  Kurata, T., Miyazaki, K., Kozuki, M., Panin, V.L., Morimoto, N., Ohta, Y., Abe, K., Atorvastatin and pitavastatin improve cognitive function and reduce senile plaque and phosphorylated tau in aged APP mice. Brain research, 1371, 161-170, 2011.
 
[13]  Shukitt-Hale, B., Cheng, V., Joseph, J.A., Effects of blackberries on motor and cognitive function in aged rats. Nutritional neuroscience, 12 (3), 135-140, 2009.
 
[14]  Ye, X., Bhupathiraju, S.N., Tucker, K.L., Variety in fruit and vegetable intake and cognitive function in middle-aged and older Puerto Rican adults. British journal of nutrition, 109 (03), 503-510, 2013.
 
[15]  Spencer, J.P., The impact of fruit flavonoids on memory and cognition. British journal of nutrition, 104 (S3), S40-S47, 2010.
 
[16]  Savage G.P., Chemical composition of walnuts (Juglans regia L.) grown in New Zealand. Plant foods for human nutrition, 56 (1): 75-82, 2001.
 
[17]  Haider, S., Batool, Z., Tabassum, S., Perveen, T., Saleem, S., Naqvi, F., Haleem, D.J., Effects of walnuts (Juglans regia) on learning and memory functions. Plant foods for human nutrition, 66 (4), 335-340, 2011.
 
[18]  Willis, L.M., Shukitt-Hale, B., Cheng, V., Joseph, J.A., Dose-dependent effects of walnuts on motor and cognitive function in aged rats. British journal of nutrition, 101 (08), 1140-1144, 2009.
 
[19]  Rodrigo, R., Miranda, A., Vergara, L., Modulation of endogenous antioxidant system by wine polyphenols in human disease. Clinica chimica acta, 412 (5), 410-424, 2011.
 
[20]  Quideau, S., Deffieux, D., Douat‐Casassus, C., Pouységu, L., Plant polyphenols: chemical properties, biological activities, and synthesis. Angewandte chemie international edition, 50 (3), 586-621, 2011.
 
[21]  Xu, Y., Zhang, J.J., Xiong, L., Zhang, L., Sun, D., Liu, H., Green tea polyphenols inhibit cognitive impairment induced by chronic cerebral hypoperfusion via modulating oxidative stress. The journal of nutritional biochemistry, 21 (8), 741-748, 2010.
 
[22]  Fernández-Fernández, L., Comes, G., Bolea, I., Valente, T., Ruiz, J., Murtra, P., Unzeta, M., LMN diet, rich in polyphenols and polyunsaturated fatty acids, improves mouse cognitive decline associated with aging and Alzheimer's disease. Behavioural brain research, 228 (2), 261-271, 2012.
 
[23]  Xu, P.X., Wang, S.W., Yu, X.L., Su, Y.J., Wang, T., Zhou, W.W., Liu, R.T., Rutin improves spatial memory in Alzheimer's disease transgenic mice by reducing Aβ oligomer level and attenuating oxidative stress and neuroinflammation. Behavioural brain research, 264, 173-180, 2014.
 
[24]  Leite, M.R., Wilhelm, E.A., Jesse, C.R., Brandão, R., Nogueira, C.W., Protective effect of caffeine and a selective A 2A receptor antagonist on impairment of memory and oxidative stress of aged rats. Experimental gerontology, 46 (4), 309-315, 2011.
 
[25]  Li, L., Tsao, R., Yang, R., Liu, C., Zhu, H., Young, J.C., Polyphenolic profiles and antioxidant activities of heartnut (Juglans ailanthifolia var. cordiformis) and Persian walnut (Juglans regia L.). Journal of agricultural and food chemistry, 54 (21), 8033-8040, 2006.
 
[26]  Ito, H., Okuda, T., Fukuda, T., Hatano, T., Yoshida, T., Two novel dicarboxylic acid derivatives and a new dimeric hydrolyzable tannin from walnuts. Journal of agricultural and food chemistry, 55 (3), 672-679, 2007.
 
[27]  Poulose, S.M., Miller, M.G., & Shukitt-Hale, B., Role of walnuts in maintaining brain health with age. The journal of nutrition, 144 (4), 561S-566S, 2014.
 
[28]  Joseph, J., Cole, G., Head, E., Ingram, D., Nutrition, brain aging, and neurodegeneration. The journal of neuroscience, 29 (41), 12795-12801, 2009.
 
[29]  Letenneur, L., Proust-Lima, C., Le Gouge, A., Dartigues, J.F., Barberger-Gateau, P., Flavonoid intake and cognitive decline over a 10-year period. American journal of epidemiology, 165 (12), 1364-1371, 2007.
 
[30]  Shaodong, C., Haihong, Z., Manting, L., Guohui, L., Zhengxiao, Z., & Zhang, Y. M., Research of influence and mechanism of combining exercise with diet control on a model of lipid metabolism rat induced by high fat diet. Lipids health disease, 12, 21, 2013.
 
[31]  Wise, L.E., Long, K.A., Abdullah, R.A., Long, J.Z., Cravatt, B.F., Lichtman, A.H., Dual fatty acid amide hydrolase and monoacylglycerol lipase blockade produces THC-like Morris water maze deficits in mice. ACS chemical neuroscience, 3 (5), 369-378, 2012.
 
[32]  Mustroph, M.L., Chen, S., Desai, S.C., Cay, E.B., DeYoung, E.K., Rhodes, J.S., Aerobic exercise is the critical variable in an enriched environment that increases hippocampal neurogenesis and water maze learning in male C57BL/6J mice. Neuroscience, 219, 62-71, 2012.
 
[33]  Harnafi, H., Ramchoun, M., Tits, M., Wauters, J.N., Frederich, M., Angenot, L., & Amrani, S., Phenolic acid-rich extract of sweet basil restores cholesterol and triglycerides metabolism in high fat diet-fed mice: A comparison with fenofibrate. Biomedicine & preventive nutrition, 3 (4), 393-397, 2013.
 
[34]  Zhang, X.L., Jiang, B., Li, Z.B., Hao, S., & An, L.J., Catalpol ameliorates cognition deficits and attenuates oxidative damage in the brain of senescent mice induced by D-galactose. Pharmacology biochemistry and behavior, 88 (1), 64-72, 2007.
 
[35]  Ōyanagui, Y., Reevaluation of assay methods and establishment of kit for superoxide dismutase activity. Analytical biochemistry, 142 (2), 290-296, 1984.
 
[36]  Hao, W., Liu, Y., Liu, S., Walter, S., Grimm, M.O., Kiliaan, A.J., Fassbender, K., Myeloid differentiation factor 88-deficient bone marrow cells improve Alzheimer’s disease-related symptoms and pathology. Brain, 134 (1), 278-292, 2011.
 
[37]  Yim, C.Y., Soczynska, J.K., Kennedy, S.H., Woldeyohannes, H.O., Brietzke, E., McIntyre, R.S., The effect of overweight/obesity on cognitive function in euthymic individuals with bipolar disorder. European psychiatry, 27(3), 223-228, 2012.
 
[38]  Kosari, S., Badoer, E., Nguyen, J.C., Killcross, A.S., Jenkins, T.A., Effect of western and high fat diets on memory and cholinergic measures in the rat. Behavioural brain research, 235(1), 98-103, 2012.
 
[39]  Li, J., Wang, C., Zhang, J.H., Cai, J.M., Cao, Y.P., Sun, X.J., Hydrogen-rich saline improves memory function in a rat model of amyloid-beta-induced Alzheimer's disease by reduction of oxidative stress. Brain research, 1328, 152-161, 2010.
 
[40]  Yu, H., Bi, Y., Ma, W., He, L., Yuan, L., Feng, J., Xiao, R., Long-term effects of high lipid and high energy diet on serum lipid, brain fatty acid composition, and memory and learning ability in mice. International journal of developmental neuroscience, 28 (3), 271-276, 2010.
 
[41]  Valls-Pedret, C., Lamuela-Raventós, R.M., Medina-Remón, A., Quintana, M., Corella, D., Pintó, X., Ros, E., Polyphenol-rich foods in the Mediterranean diet are associated with better cognitive function in elderly subjects at high cardiovascular risk. Journal of Alzheimer's disease, 29 (4), 773-782, 2012.
 
[42]  Spencer, J.P., Vauzour, D., Rendeiro, C., Flavonoids and cognition: the molecular mechanisms underlying their behavioural effects. Archives of biochemistry and biophysics, 492 (1), 1-9, 2009.
 
[43]  Papandreou, M.A., Dimakopoulou, A., Linardaki, Z.I., Cordopatis, P., Klimis-Zacas, D., Margarity, M., Lamari, F.N., Effect of a polyphenol-rich wild blueberry extract on cognitive performance of mice, brain antioxidant markers and acetylcholinesterase activity. Behavioural brain research, 198 (2), 352-358, 2009.
 
[44]  Martinello, F., Soares, S.M., Franco, J.J., Santos, A.C., Sugohara, A., Garcia, S.B., & Uyemura, S.A., Hypolipemic and antioxidant activities from Tamarindus indica L. pulp fruit extract in hypercholesterolemic hamsters. Food and chemical toxicology, 44 (6), 810-818, 2006.
 
[45]  Chung, M.J., Sung, N.J., Park, C.S., Kweon, D.K., Mantovani, A., Moon, T.W., & Park, K.H., Antioxidative and hypocholesterolemic activities of water-soluble puerarin glycosides in HepG2 cells and in C57 BL/6J mice. European journal of pharmacology, 578 (2), 159-170, 2008.
 
[46]  Yang, R., Le, G., Li, A., Zheng, J., & Shi, Y., Effect of antioxidant capacity on blood lipid metabolism and lipoprotein lipase activity of rats fed a high-fat diet. Nutrition, 22 (11), 1185-1191, 2006.
 
[47]  Elias, M.F., Elias, P.K., Sullivan, L.M., Wolf, P.A., D'agostino, R.B., Lower cognitive function in the presence of obesity and hypertension: the Framingham heart study. International journal of obesity, 27 (2), 260-268, 2003.
 
[48]  Farr, S.A., Yamada, K.A., Butterfield, D.A., Abdul, H.M., Xu, L., Miller, N.E., Morley, J.E., Obesity and hypertriglyceridemia produce cognitive impairment. Endocrinology, 149 (5), 2628-2636, 2008.
 
[49]  Butterfield, D.A., Drake, J., Pocernich, C., Castegna, A., Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid β-peptide. Trends in molecular medicine, 7(12), 548-554, 2001.
 
[50]  Khan, R.A., Khan, M.R., Sahreen, S., Protective effects of rutin against potassium bromate induced nephrotoxicity in rats. BMC complementary and alternative medicine, 12 (1), 204, 2012.
 
[51]  Zhang, X.L., Jiang, B., Li, Z.B., Hao, S., An, L.J., Catalpol ameliorates cognition deficits and attenuates oxidative damage in the brain of senescent mice induced by D-galactose. Pharmacology biochemistry and behavior, 88 (1), 64-72, 2007.
 
[52]  Fukuda, T., Ito, H., & Yoshida, T., Antioxidative polyphenols from walnuts (<i> Juglans regia</i> L.). Phytochemistry, 63 (7), 795-801, 2003.
 
[53]  Pribis, P., Bailey, R.N., Russell, A.A., Kilsby, M.A., Hernandez, M., Craig, W.J., & Sabate, J., Effects of walnut consumption on cognitive performance in young adults. British journal of nutrition, 107 (09), 1393-1401, 2012.
 
[54]  Poulose, S.M., Miller, M.G., & Shukitt-Hale, B., Role of walnuts in maintaining brain health with age. The journal of nutrition, 144 (4), 561S-566S, 2014.
 
[55]  Shabani, M., Nazeri, M., Parsania, S., Razavinasab, M., Zangiabadi, N., Esmaeilpour, K., & Abareghi, F., Walnut consumption protects rats against cisplatin-induced neurotoxicity. Neurotoxicology, 33 (5), 1314-1321, 2012.
 
[56]  Ramassamy, C., Emerging role of polyphenolic compounds in the treatment of neurodegenerative diseases: a review of their intracellular targets. European journal of pharmacology, 545 (1), 51-64, 2006.
 
[57]  Moreira, E.L.G., Aguiar Jr, A.S., de Carvalho, C.R., Santos, D.B., de Oliveira, J., de Bem, A.F., Prediger, R.D., Effects of lifestyle modifications on cognitive impairments in a mouse model of hypercholesterolemia. Neuroscience letters, 541, 193-198, 2013.
 
[58]  Umeda, T., Tomiyama, T., Kitajima, E., Idomoto, T., Nomura, S., Lambert, M.P., Mori, H., Hypercholesterolemia accelerates intraneuronal accumulation of Aβ oligomers resulting in memory impairment in Alzheimer's disease model mice. Life sciences, 91 (23), 1169-1176, 2012.