Walnut Polyphenols Inhibit Pancreatic Lipase Activity in Vitro and Have Hypolipidemic Effect on High-Fat Diet-Induced Obese Mice

Dandan Shi¹, Chaoyin Chen^1, , Shenglan Zhao^2, , 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

Cite this paper:
Dandan Shi, Chaoyin Chen, Shenglan Zhao, Feng Ge, Diqiu Liu and Hao Song. Walnut Polyphenols Inhibit Pancreatic Lipase Activity in Vitro and Have Hypolipidemic Effect on High-Fat Diet-Induced Obese Mice. Journal of Food and Nutrition Research. 2014; 2(10):757-763. doi: 10.12691/jfnr-2-10-16

Abstract

This study was aimed at the chemical composition and inhibitory effects of walnut polyphenols (WP) in vitro lipase activity and on obesity in obese mice models. More than 20 individual phenolics such as gallotannins, ellagitannins, flavonoids and phenolic acids were identified in WP. Studying the interactions between porcine pancreatic lipase (PL) and WP were based on fluorescence quenching and an enzymatic assay. The addition of WP to lipase caused a reduction of protein fluorescence intensity at 310 K. In addtion, we found that the effect of WP on PL was dependent on reaction medium and substrate used and the half maximal inhibitory concentration of WP was determined to be 163 μg/mL. At the beginning of the experiment, mice were divided into 3 groups, one of them served as normal control group (NCG), the second as hyperlipidemia control group (HCG), the last as walnut polyphenol-treated group (WTG). After 8 weeks of treatment, we investigated the effects of WP on weight gain, food intake and biochemical indexes in obese mice. The results showed that WP could significantly decrease body weight in obese mice (-13.52%, P < 0.05). However, there was no remarkable difference in food intake among three groups (1760.2–1823.3 g). In addition, WP could significantly decrease the TG, TC and LDL-cholesterol (LDL-C) concentrations and increase the HDL-cholesterol (HDL-C) concentration when compared to the HCG (-36.12%, -31.27%, -73.3%, and +59.72%, respectively, P < 0.01). The levels of hepatic TG and TC were significantly decrease in WTG when compared to the HCG (-27.72% and -48.43%, respectively, P < 0.01). In conclusion, these results suggest that WP could be a potentially therapeutic alternative in the treatment of obesity caused by a high-fat diet.

Keywords:
walnut polyphenols lipase fluorescence quenching obese mice

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References:

[1]	Pataky, Z., Bobbioni-Harsch, E., Hadengue, A., Carpentier, A., & Golay, A., . Revue medicale suisse, 5 (196), 662-4, 2009.
[2]	Nakai, M., Fukui, Y., Asami, S., Toyoda-Ono, Y., Iwashita, T., Shibata, H., Kiso, Y., Inhibitory effects of oolong tea polyphenols on pancreatic lipase in vitro. Journal of Agricultural and Food Chemistry, 53 (11), 4593-4598, 2005.
[3]	Yun, J.W., Possible anti-obesity therapeutics from nature–A review. Phytochemistry, 71 (14), 1625-1641, 2010.
[4]	Zhang, J., Xiao, L., Yang, Y., Wang, Z., & Li, G., Lignin binding to pancreatic lipase and its influence on enzymatic activity. Food chemistry, 149, 99-106, 2014.
[5]	Birari, R.B., & Bhutani, K.K., Pancreatic lipase inhibitors from natural sources: unexplored potential. Drug discovery today, 12 (19), 879-889, 2007.
[6]	Thomson, A.B.R., De Pover, A., Keelan, M., Jarocka-Cyrta, E., & Clandinin, M.T., Inhibition of lipid absorption as an approach to the treatment of obesity. Methods in enzymology, 286, 3-44, 1997.
[7]	Garza, A.L., Milagro, F.I., Boque, N., Campión, J., & Martinez, J. A., Natural inhibitors of pancreatic lipase as new players in obesity treatment, 77 (8), 773-785, 2011.
[8]	Bhutani, K.K., Birari, R., & Kapat, K., Potential anti-obesity and lipid lowering natural products: a review. Natural Product Communications, 2 (3), 331-348, 2007.
[9]	Sumithran, P., & Proietto, J., Benefit-Risk Assessment of Orlistat in the Treatment of Obesity. Drug Safety, 1-12, 2014.
[10]	Kawaguchi, K., Mizuno, T., Aida, K., & Uchino, K., Hesperidin as an inhibitor of lipases from porcine pancreas and Pseudomonas. Bioscience, biotechnology, and biochemistry, 61 (1), 102-104, 1997.
[11]	Won, S.R., Kim, S.K., Kim, Y.M., Lee, P.H., Ryu, J.H., Kim, J.W., & Rhee, H.I., Licochalcone A: A lipase inhibitor from the roots of Glycyrrhiza uralensis, Food research international, 40 (8), 1046-1050, 2007.
[12]	Rastmanesh, R., High polyphenol, low probiotic diet for weight loss because of intestinal microbiota interaction. Chemico-biological interactions, 189 (1), 1-8, 2011.
[13]	Schaefer, S., Baum, M., Eisenbrand, G., Dietrich, H., Will, F., & Janzowski, C., Polyphenolic apple juice extracts and their major constituents reduce oxidative damage in human colon cell lines. Molecular nutrition & food research, 50 (1), 24-33, 2006.
[14]	McDougall, G.J., & Stewart, D., The inhibitory effects of berry polyphenols on digestive enzymes. Biofactors, 23 (4), 189-195, 2005.
[15]	Sakulnarmrat, K., Srzednicki, G., & Konczak, I., Composition and inhibitory activities towards digestive enzymes of polyphenolic-rich fractions of Davidson's plum and quandong. LWT-Food Science and Technology, 57 (1), 366-375, 2014.
[16]	Wang, S., Dong, S., Zhang, R., Shao, H., & Liu, Y., Effects of proanthocyanidins on porcine pancreatic lipase: Conformation, activity, kinetics and thermodynamics. Process Biochemistry, 49 (2), 237-243, 2014.
[17]	Meydani, M., & Hasan, S.T., Dietary polyphenols and obesity. Nutrients, 2 (7), 737-751, 2010.
[18]	Ainsworth, E.A., & Gillespie, K.M., Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent. Nature protocols, 2 (4), 875-877, 2007.
[19]	Regueiro, J., Sánchez-González, C., Vallverdú-Queralt, A., Simal-Gándara, J., Lamuela-Raventós, R., & Izquierdo-Pulido, M., Comprehensive identification of walnut polyphenols by liquid chromatography coupled to linear ion trap–Orbitrap mass spectrometry. Food chemistry, 152, 340-348, 2014.
[20]	Ojha, H., Mishra, K., Hassan, M.I., & Chaudhury, N.K., Spectroscopic and isothermal titration calorimetry studies of binding interaction of ferulic acid with bovine serum albumin. Thermochimica Acta, 548, 56-64, 2012.
[21]	McDougall, G.J., Kulkarni, N.N., & Stewart, D., Berry polyphenols inhibit pancreatic lipase activity in vitro. Food Chemistry, 115 (1), 193-199, 2009.
[22]	Martins, F., Noso, T.M., Porto, V.B., Curiel, A., Gambero, A., Bastos, D.H., & Carvalho, P.D.O., Maté Tea Inhibits In Vitro Pancreatic Lipase Activity and Has Hypolipidemic Effect on High–fat Diet–induced Obese Mice. Obesity, 18 (1), 42-47, 2010.
[23]	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 Dis, 12, 21, 2013.
[24]	Honda, H., Ikejima, K., Hirose, M., Yoshikawa, M., Lang, T., Enomoto, N., & Sato, N., Leptin is required for fibrogenic responses induced by thioacetamide in the murine liver. Hepatology, 36 (1), 12-21, 2002.
[25]	Yuan, H., Song, J., Li, X., Li, N., & Dai, J., Immunomodulation and antitumor activity of κ-carrageenan oligosaccharides. Cancer letters, 243 (2), 228-234, 2006.
[26]	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.
[27]	Shimoda, H., Tanaka, J., Kikuchi, M., Fukuda, T., Ito, H., Hatano, T., & Yoshida, T., Effect of polyphenol-rich extract from walnut on diet-induced hypertriglyceridemia in mice via enhancement of fatty acid oxidation in the liver. Journal of agricultural and food chemistry, 57 (5), 1786-1792, 2009.
[28]	Jang, D.S., Lee, G.Y., Kim, J., Lee, Y.M., Kim, J.M., Kim, Y.S., & Kim, J.S., A new pancreatic lipase inhibitor isolated from the roots of Actinidia arguta. Archives of pharmacal research, 31 (5), 666-670, 2008.
[29]	Lakowicz, J.R., & Masters, B.R., Principles of fluorescence spectroscopy. Journal of Biomedical Optics, 13(2), 9901, 2008.
[30]	Wu, X., He, W., Zhang, H., Li, Y., Liu, Z., & He, Z., Acteoside: A lipase inhibitor from the Chinese tea Ligustrum purpurascens kudingcha. Food chemistry, 142, 306-310, 2014.
[31]	Stojadinovic, M., Radosavljevic, J., Ognjenovic, J., Vesic, J., Prodic, I., Stanic-Vucinic, D., & Cirkovic Velickovic, T., Binding affinity between dietary polyphenols and β-lactoglobulin negatively correlates with the protein susceptibility to digestion and total antioxidant activity of complexes formed. Food chemistry, 136 (3), 1263-1271, 2013.
[32]	Augustin, M.A., Sanguansri, L., & Lockett, T., Nano-and micro-encapsulated systems for enhancing the delivery of resveratrol. Annals of the New York Academy of Sciences, 1290 (1), 107-112, 2013.
[33]	Tayeh, N., Rungassamy, T., & Albani, J.R., Fluorescence spectral resolution of tryptophan residues in bovine and human serum albumins. Journal of pharmaceutical and biomedical analysis, 50 (2), 107-116, 2009.
[34]	Herrmann, K., & Nagel, C.W., Occurrence and content of hydroxycinnamic and hydroxybenzoic acid compounds in foods. Critical Reviews in Food Science & Nutrition, 28 (4), 315-347, 1989.
[35]	Ignat, I., Volf, I., & Popa, V.I., A critical review of methods for characterisation of polyphenolic compounds in fruits and vegetables. Food Chemistry, 126 (4), 1821-1835, 2011.
[36]	Moreno, S., Scheyer, T., Romano, C.S., & Vojnov, A.A., Antioxidant and antimicrobial activities of rosemary extracts linked to their polyphenol composition. Free radical research, 40 (2), 223-231, 2006.
[37]	Nakai, M., Fukui, Y., Asami, S., Toyoda-Ono, Y., Iwashita, T., Shibata, H., & Kiso, Y., Inhibitory effects of oolong tea polyphenols on pancreatic lipase in vitro. Journal of Agricultural and Food Chemistry, 53 (11), 4593-4598, 2005.
[38]	Määttä-Riihinen, K.R., Kamal-Eldin, A., Mattila, P.H., González-Paramás, A.M., & Törrönen, A.R., Distribution and contents of phenolic compounds in eighteen Scandinavian berry species. Journal of Agricultural and Food Chemistry, 52 (14), 4477-4486, 2004.
[39]	Raghavendra, M.P., Kumar, P.R., & Prakash, V., Mechanism of inhibition of rice bran lipase by polyphenols: a case study with chlorogenic acid and caffeic acid. Journal of food science, 72(8), E412-E419, 2007.
[40]	Wu, T., Qi, X., Liu, Y., Guo, J., Zhu, R., Chen, W., & Yu, T., Dietary supplementation with purified mulberry (Morus australis Poir) anthocyanins suppresses body weight gain in high-fat diet fed C57BL/6 mice. Food chemistry, 141 (1), 482-487, 2013.
[41]	Westerterp-Plantenga, M.S., Lejeune, M.P., & Kovacs, E.M., Body weight loss and weight maintenance in relation to habitual caffeine intake and green tea supplementation. Obesity research, 13 (7), 1195-1204, 2005.
[42]	Cho, A.S., Jeon, S.M., Kim, M.J., Yeo, J., Seo, K.I., Choi, M.S., & Lee, M.K., Chlorogenic acid exhibits anti-obesity property and improves lipid metabolism in high-fat diet-induced-obese mice. Food and Chemical Toxicology, 48 (3), 937-943, 2010.
[43]	Pang, J., Choi, Y., & Park, T., Ilex paraguariensis extract ameliorates obesity induced by high-fat diet: Potential role of AMPK in the visceral adipose tissue. Archives of biochemistry and biophysics, 476 (2), 178-185, 2008.
[44]	Wu, C.H., Yang, M.Y., Chan, K.C., Chung, P.J., Ou, T.T., & Wang, C.J., Improvement in high-fat diet-induced obesity and body fat accumulation by a Nelumbo nucifera leaf flavonoid-rich extract in mice. Journal of agricultural and food chemistry, 58 (11), 7075-7081, 2010.
[45]	Shi, D., Chen, C., Zhao, S., Ge, F., Liu, D., & Song, H., Effects of Walnut Polyphenol on Learning and Memory Functions in Hypercholesterolemia Mice. Journal of Food and Nutrition Research, 2 (8), 450-456, 2014.