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Tetragonia Tetragonoides (Pall.) Kuntze (New Zealand Spinach) Prevents Obesity and Hyperuricemia in High-Fat Diet-Induced Obese Mice

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Tetragonia Tetragonoides (Pall.) Kuntze (New Zealand Spinach) Prevents Obesity and Hyperuricemia in High-Fat Diet-Induced Obese Mice nutrients Article Tetragonia tetragonoides (Pall.) Kuntze (New Zealand Spinach) Prevents Obesity and Hyperuricemia in High-Fat Diet-Induced Obese Mice Young-Sil Lee 1, Seung-Hyung Kim 2 ID , Heung Joo Yuk 1, Geung-Joo Lee 3,* and Dong-Seon Kim 1,* 1 Herbal Medicine Research Division, Korea Institute of Oriental Medicine, 1672 Yuseong-daero, Yuseong-gu, Dajeon 34054, Korea; [email protected] (Y.-S.L.); [email protected] (H.J.Y.) 2 Institute of Traditional Medicine and Bioscience, Daejeon University, 62 Daehak-ro, Dong-gu, Daejeon 34520, Korea; [email protected] 3 Department of Horticulture, Chungnam National University, 99 Daehak-ro, Yuseong-gu, Daejeon 34134, Korea * Correspondence: [email protected] (G.-J.L.); [email protected] (D.-S.K.); Tel.: +82-42-821-5734 (G.-J.L.); +82-42-868-9639 (D.-S.K.) Received: 6 July 2018; Accepted: 10 August 2018; Published: 14 August 2018 Abstract: Tetragonia tetragonoides (Pall.) Kuntze, called New Zealand spinach (NZS), is an edible plant used in salad in Western countries and has been used to treat gastrointestinal diseases in traditional medicine. We examined the anti-obesity and anti-hyperuricemic effects of NZS and the underlying mechanisms in high-fat diet (HFD)-induced obese mice. Mice were fed a normal-fat diet (NFD); high-fat diet (HFD); HFD with 75, 150, or 300 mg/kg NZS extract; or 245 mg/kg Garcinia cambogia (GC) extract. NZS decreased body weight gain, total white adipose tissue (WAT), liver weight, and size of adipocytes and improved hepatic and plasma lipid profiles. With NZS, the plasma levels of the leptin and uric acid were significantly decreased while the levels of the adiponectin were increased. Furthermore, NZS decreased the expression levels of adipogenesis-related genes and xanthine oxidoreductase (XOR), which is involved in uric acid production, while increasing that of proteins associated with fatty acid oxidation. UPLC analysis 000 00 revealed that NZS contained 6-methoxykaempferol-3-O-β-D-glucosyl(1 !2 )-β-D-glucopyranoside, 000 00 0000 6-methoxykaempferol-3-O-β-D-glucosyl(1 !2 )-β-D-glucopyranosyl-(6 -caffeoyl)-7-O-β-D- 0 000 00 glucopyranoside, and 6,4 -dimethoxykaempferol-3-O-β-D-glucosyl(1 !2 )-β-D-glucopyranosyl- 0000 (6 -caffeoyl)-7-O-β-D-glucopyranoside. These results suggest that NZS exerts anti-obesity, anti-hyperlipidemia, and anti-hyperuricemic effects in HFD-induced obese mice, which are partly explained by regulation of lipid-metabolism-related genes and proteins and decreased expression of XOR. Keywords: Tetragonia tetragonoides (Pall.) Kuntze; obesity; hyperuricemia; lipogenesis; fatty acid oxidation; xanthine oxidoreductase 1. Introduction Obesity is a serious public health problem that threatens human health worldwide. It results from abnormalities in energy metabolism in adipose tissue, which leads to increased fat mass in tissues, such as adipose tissue and liver tissue, and elevated lipids levels in the blood [1,2]. Obesity is associated with the development of metabolic disorders, such as type 2 diabetes, hyperlipidemia, fatty liver, hypertension, and cardiovascular disease [3,4]. Hyperuricemia is characterized by elevated blood uric acid levels, the final product of purine metabolism. Uric acid plays an important role in Nutrients 2018, 10, 1087; doi:10.3390/nu10081087 www.mdpi.com/journal/nutrients Nutrients 2018, 10, 1087 2 of 16 the development of metabolic disorders, since uric acid regulates the oxidative stress, inflammation, and proteins involved in glucose and lipid metabolism, and hyperuricemia is positively associated with increased visceral fat mass and various metabolic disorders, such as dyslipidemia, type 2 diabetes, and atherosclerosis [4,5]. Especially, uric acid production in adipose tissue is accompanied by increased xanthine oxidoreductase (XOR) activity, which degrades hypoxanthine and xanthine to uric acid. XOR expression and activity is associated with increased obesity and regulation of adipogenesis in adipose tissue [6,7]. It is considered one of the metabolic diseases linked to both obesity and various metabolic disorders, and growing attention is being paid to the relationship between obesity and uric acid metabolism [5,8]. Although pharmacological therapies are used in clinical practices to treat obesity and hyperuricemia, their use is limited by undesirable side effects [9,10]. Thus, new research on food and drugs that can overcome these limitations is needed. Therefore, increasing attention has been paid to natural products, including traditional medicines, as an alternative strategy [11]. Tetragonia tetragonoides (Pall.) Kuntze, called New Zealand spinach (NZS), is a perennial plant belonging to the Aizoaceae family. It is an edible plant used in salads in Western countries. In Korean medicine, T. tetragonoides has been used as a herbal medicine to treat gastrointestinal diseases, such as gastric hypersecretion, dyspepsia, gastric ulcer, and gastritis [12]. Recently, T. tetragonoides has been reported to improve women’s health, regulate glucose metabolism, and exert anti-inflammatory effects [13,14]. To date, there are no reports available on the effects of T. tetragonoides on obesity, lipid accumulation, or uric acid metabolism. In the present study, we examined the anti-obesity and anti-hyperuricemic effects of NZS and their underlying mechanisms in high-fat diet (HFD)-induced obese mice. 2. Materials and Methods 2.1. Preparation of NZS Extracts T. tetragonoides (Pall.) Kuntze (NZS) leaves were collected from the ocean sand dunes of Shinan-gun, Jeonnam Province, Korea. The plants were identified by Professor Geung-Joo Lee (Department of Horticulture, Chungnam National University, Daejeon, Korea). An extract from NZS leaves (dry weight, 1 kg) was prepared with 70% ethanol under reflux in a condensation system at 85 ◦C for 3 h. The extract was concentrated under reduced pressure using a rotary evaporator and then lyophilized. The yield of the dried extract from the starting crude material was 11.2%. 2.2. Animal Study Four-week-old male C57BL/6J mice were purchased from Daehan Biolink Co. (Eumsung, Korea). The mice were maintained under controlled temperature (23 ± 3 ◦C) and humidity (50%) conditions with a 12-h light/dark cycle. After 1 week of acclimatization, the mice were divided into one of the following six groups based on body weight: group 1 (normal-fat diet (NFD), n = 5) was fed a standard chow diet (14% fat, 21% protein, and 65% carbohydrate; Orient Bio Inc., Seongnam, Korea); group 2 (high-fat diet (HFD), n = 5) was fed a high-fat diet (60% fat, 20% protein, and 20% carbohydrate; rodent diet D12492, Research Diets, New Brunswick, NJ, USA); groups 3, 4, and 5 (HFD + NZS 75, 150, and 300, n = 5, respectively) were fed an HFD and given NZS at doses of 75, 150, and 300 mg/kg, respectively; and group 6 (HFD + Garcinia cambogia (GC), n = 5) was fed an HFD and given Garcinia cambogia (GC) extract at a dose of 245 mg/kg as a positive control. NZS and GC were dissolved in a vehicle (0.5% carboxylmethylcellulose) and orally administered once daily for 8 weeks. Mice in the NFD and HFD groups were administered the vehicle alone. The mice were allowed free access to water and food, and the body weights and food intake were measured every week. Food efficiency rate was calculated as (total weight gain/total food intake) × 100. The experimental design was approved by the Institutional Animal Care and Use Committee of Daejeon University, and all experiments were performed in accordance with committee guidelines. Nutrients 2018, 10, 1087 3 of 16 2.3. Blood Collection and Biochemical Analyses of Plasma After 8 weeks, the mice were euthanized with ether after overnight fasting. Blood samples were collected by cardiac puncture and centrifuged to obtain plasma, and separated plasma samples were stored at −80 ◦C until use. Plasma glucose, triglyceride (TG), non-esterified fatty acid (NEFA), total cholesterol (T-CHO), low-density lipoprotein cholesterol (LDL-CHO), and high-density lipoprotein cholesterol (HDL-CHO) were analyzed using an automatic biochemical analyzer (Hitachi-7020, Hitachi Medical, Tokyo, Japan). Plasma uric acid levels were determined with a colorimetric assay kit (BioVision, Milpitas, CA, USA). Plasma leptin and adiponectin levels were measured by immunoassay using ELISA kits (Mouse Leptin and Adiponectin/Acrp30; R&D Systems, Minneapolis, MN, USA) according to the manufacturer’s protocols and presented corrected by total white adipose tissue (WAT) weight. 2.4. Tissue Collection and Histological Analysis Liver and white adipose tissue (WAT; epididymal, perirenal, mesenteric, and subcutaneous WAT) were dissected immediately, rinsed, weighed, frozen in liquid nitrogen, and stored at −80 ◦C until analysis. For histological examination, the liver and WAT were fixed in a 10% formalin solution and embedded in paraffin. Sections were stained with hematoxylin and eosin (H&E). Adipocyte size was determined by measuring the area taken up by 20 adipocytes in a stained section and adipocyte cell number was measured by Image J1.49 software (http://rsb.info.nih.gov/ij/download.html). To determine liver lipid accumulation, liver sections were stained with Oil-red O and hematoxylin. 2.5. Measurement of Liver TG Levels Liver tissue (0.1 g) was homogenized in 95% ethanol and centrifuged. The resulting supernatant was mixed with sodium chlorate and triton X-100. TG levels were determined using a commercial kit (Triglyceride E test, Wako Pure Chemical Industries, Osaka, Japan) according to the manufacturer’s protocol. 2.6. Total RNA Isolation and Gene Expression Analyses Total RNA was isolated from WAT of mice with the TRI reagent (Sigma-Aldrich Co., St. Louis, MO, USA) and reverse-transcribed to cDNA with an oligo primer using a FirstStand cDNA synthesis kit (Amersham Pharmacia, Piscataway, NJ, USA) according to the manufacturer’s protocol. The mRNA expression levels of adipogenesis-related genes were analyzed using gene-specific primers, probes, Power SYBR® Green PCR Master Mix, and TaqMan® Gene E-expression Master Mix (Applied Biosystems, Foster City, CA, USA) according to the manufacturer’s instructions using a real-time PCR ABI Prism 7700 system (Applied Biosystems).
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