Ilex paraguariensis A.St.-Hil. improves lipid metabolism in high-fat diet-fed obese rats and suppresses intracellular lipid accumulation in 3T3-L1 adipocytes via the AMPK-dependent and insulin signaling pathways

  • Maya Kudo School of Pharmacy and Pharmaceutical Science, Mukogawa Women’s University, Nishinomiya, Hyogo, Japan
  • Ming Gao School of Pharmacy and Pharmaceutical Science, Mukogawa Women’s University, Nishinomiya, Hyogo, Japan; and Institute for Bioscience, Mukogawa Women’s University, Nishinomiya, Hyogo, Japan
  • Misa Hayashi School of Pharmacy and Pharmaceutical Science, Mukogawa Women’s University, Nishinomiya, Hyogo, Japan
  • Yukiko Kobayashi Tokiwa Phytochemical Co., Ltd., Sakura, Chiba, Japan
  • Jinwei Yang Tokiwa Phytochemical Co., Ltd., Sakura, Chiba, Japan
  • Tonghua Liu Key Laboratory of Health Cultivation of the Ministry of Education, Beijing University of Chinese Medicine, Beijing, China
Keywords: mate, life-style-related diseases, adipose tissue, adipogenesis, lipolysis, lipid metabolism pathway

Abstract

Background: Obesity is closely associated with several chronic diseases, and adipose tissue plays a major role in modulating energy metabolism.

Objective: This study aimed to determine whether Mate, derived from I. paraguariensis A.St.-Hil., ameliorates lipid metabolism in 3T3-L1 adipocytes and high-fat diet (HFD)-fed obese Sprague-Dawley (SD) rats.

Design: 3T3-L1 adipocytes were cultured for 7 days, following which intracellular lipid accumulation and expression levels of lipid metabolism-related factors were examined. Dorsomorphin was used to investigate the potential pathways involved, particularly the adenosine monophosphate-activated protein kinase (AMPK)- dependent pathway. Mate was administered to rat HFD-fed obese SD models for 8 consecutive weeks. The expression of lipid metabolism-related factors in the organs and tissues collected from dissected SD rats was evaluated.

Results: Mate suppressed intracellular lipid accumulation in 3T3-L1 adipocytes, increased the protein and gene expression levels of AMPK, hormone sensitive lipase (HSL), calmodulin kinase kinase (CaMKK), liver kinase B1 (LKB1), protein kinase A (PKA), CCAAT/enhancer binding protein β (C/EBPβ), insulin receptor b (IRβ), and insulin receptor substrate 1 (IRS1) (Tyr465), and decreased those of sterol regulatory element binding protein 1C (Srebp1c), fatty acid synthase (FAS), peroxisome-activated receptor γ (PPARγ), and IRS1 (Ser1101). Furthermore, an AMPK inhibitor abolished the effects exerted by Mate on intracellular lipid accumulation and HSL and FAS expression levels. Mate treatment suppressed body weight gain and improved serum cholesterol levels in HFD-fed obese SD rats. Treatment with Mate increased the protein and gene expression levels of AMPK, PKA, Erk1/Erk2 (p44/p42), and uncoupling protein 1 and reduced those of mammalian target of rapamycin, S6 kinase, Srebp1c, ap2, FAS, Il6, Adiponectin, Leptin, and Fabp4 in rat HFD-fed obese SD models.

Discussion and conclusions: Mate suppressed intracellular lipid accumulation in 3T3-L1 adipocytes and improved lipid metabolism in the epididymal adipose tissue of HFD-fed obese SD rats via the activation of AMPK-dependent and insulin signaling pathways.

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References


1.
Jiang D, Wang D, Zhuang X, Wang Z, Ni Y, Chen S, et al Berberine increases adipose triglyceride lipase in 3T3-L1 adipocytes through the AMPK pathway. Lipids Health Dis 2016; 15: 214. doi: 10.1186/s12944-016-0383-4


2.
Kopelman PG. Obesity as s medical problem. Nature 2000; 404: 635–43. doi: 10.1038/35007508


3.
Hotamisligil GS, Erbay E. Nutrient sensing and inflammation in metabolic diseases. Nat Rev Immunol 2008; 8: 923–34. doi: 10.1038/nri2449


4.
Kang YM, Kang HA, Cominguez DC, Kim SH, An HJ. Papain ameliorates lipid accumulation and inflammation in high-fat diet-induced obesity mice and 3T3-L1 adipocytes via AMPK activation. Int J Mol Sci 2021; 22: 9885. doi: 10.3390/ijms22189885


5.
Kang JG, Park CK. Anti-obesity drugs: a review about their effects and safety. Diabetes Metab J 2012; 36: 13–25. doi: 10.4093/dmj.2012.36.1.13


6.
Karri S, Sharma S, Hatware K, Patil K. Natural anti-obesity agents and their therapeutic role in management of obesity: a future trend perspective. Biomed Pharmacother 2019; 110: 224–38. doi: 10.1016/j.biopha.2018.11.076


7.
Cheng L, Zhang S, Shang F, Ning Y, Huang Z, He R, et al. Emodin improves glucose and lipid metabolism disorders in obese mice via activating brown adipose tissue and inducing browning of white adipose tissue. Front Endocrinol 2021; 10: 20: 618037. doi: 10.22541/au.159542439.92776214


8.
Tran TT, Kahn CR. Transplantation of adipose tissue and stem cells: role on metabolism and disease. Nat Rev Endocrinol 2010; 6: 195–215. doi: 10.1038/nrendo.2010.20


9.
Wang C, Li JX, Xue HF, Li Y, Huang JF, Mai JZ, et al. Type 2 diabetes mellitus incidence in Chinese: contributions of overweight and obesity. Diabetes Res Clin Pract 2015; 107: 424–32. doi: 10.1016/j.diabres.2014.09.059


10.
Bu S, Yuan CY, Xue Q, Chen Y, Cao F. Bilobalide suppresses adipogenesis in 3T3-L1 adipocytes via the AMPK signaling pathway. Molecules 2019; 24: 3503. doi: 10.3390/molecules24193503


11.
Bijland S, Mancini S. J, Salt I. P. Role of AMP-activated protein kinase in adipose tissue metabolism and inflammation. Clin Sci 2013; 124: 491–507. doi: 10.1042/CS20120536


12.
Ma C, Li G, He Y, Xu B, Mi X, Wang H, et al. Pronuciferine and nucuferine inhibit lipogenesis in 3T3-L1 adipocytes by activating the AMPK signaling pathway. Life Sci 2015; 136: 120–5. doi: 10.1016/j.lfs.2015.07.001


13.
Chen Z, Shen X, Shen F, Zhong W, Wu H, Liu S, et al. TAK1 activates AMPK-dependent cell death pathway in hydrogen peroxide-treated cardiomyocytes, inhibited by heart shock protein-70. Mol Cell Biochem 2013; 377: 35–44. doi: 10.1007/s11010-013-1568-z


14.
Shaw RJ, Lamia KA, Vasquez D, Koo SH, Bardeesy N, Depinho RA, et al. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science 2005; 310: 1642–6. doi: 10.1126/science.1120781


15.
Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR, et al. Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2005; 2: 21–33. doi: 10.1016/j.cmet.2005.06.005


16.
Wang Q, Liu S, Zhai A, Zhang B, Tian G. AMPK-mediated regulation of lipid metabolism by phosphorylation. Biol Pharm Bill 2018; 41: 985–93. doi: 10.1248/bpb.b17-00724


17.
Munday MR. Regulation of mammalian acetyl-CoA carboxylase. Biochem Soc Trans 2002; 30: 1059–64.


18.
Wang Y, Viscarra J, Kim SJ, Sul HS. Transcriptional regulation of hepatic lipogenesis. Nat Rev Mol Cell Biol 2015; 16: 678–89.


19.
Moseti D, Regassa A, Kim WK. Molecular regulation of adipogenesis and potential anti-adipogenic bioactive molecules. Int J Mol Sci 2016; 17: 124. doi: 10.3390/ijms17010124


20.
Wu Z, Rosen ED, Brun R, Hauser S, Adelmant G, Troy AE, et al. Cross regulation of C/EBP alpha and PPAR gamma controls the transcriptional pathway of adipogenesis and insulin sensitivity. Mol Cell 1999; 3: 151–8. doi: 10.1016/S1097-2765(00)80306-8


21.
Hwang KA, Hwang YJ, Im PR, Hwang HJ, Song J, Kim YJ. Platycodon grandiflorum extract reduces high-fat diet-induced obesity through regulation of adipogenesis and lipogenesis pathways in mice. J Med Food 2019; 22: 993–9.


22.
Lee JH, Woo KJ, Kim MA, Hong J, Kim J, Kin SH, et al. Heat-killed Enterococcus faecalis prevents adipogenesis and high fat diet-induced obesity by inhibition of lipid accumulation through inhibiting C/EBP-α and PPAR-γ in the insulin signaling pathway. Nutrients 2022; 14: 1308. doi: 10.3390/nu14061308


23.
Horiuchi H, Kamikado K, Aoki R, Suganuma N, Nishijima T, Nakatani A, et al. Bufidobacterium animalis subsp. lactis GCL2505 modulates host energy metabolism via the short-chain fatty receptor GPR43. Sci Reo 2020; 10: 1–8. doi: 10.1038/s41598-020-60984-6


24.
Seo M, Lee Y, Hwang JH, Kim K, Lee BY. The inhibitory effects of quercetin on obesity and obesity-induced inflammation by regulation of MAPK signaling. J Nutr Biochem 2015; 26: 1308–16. doi: 10.1016/j.jnutbio.2015.06.005


25.
Balaktishnan BB. Krishnasamy K, Choi KC. Moringa concanensis NImmo ameliorates hyperglycemia in 3T3-L1 adipocytes by upregulating PPAR-γ, C/EBP-α via Akt signaling pathway and STZ- induced diabetic rats. Biomed Pharmacother 2018; 103: 719–28. doi: 10.1016/j.biopha.2018.04.047


26.
Carmo LS, Rogero MM, Cortez M, Yamada M, Jacob RS, Bastos DHM, et al. The effects of Yerba Maté (Ilex Paraguariensis) consumption on IL-1, IL-6, TNF-α and IL-10 production by bone marrow cells in Wistar rats fed a high-fat diet. Int J Vitam Res 2013; 83(1): 26–35.


27.
Heck CI, de Mejia EG. Yerba Mate Tea (Ilex paraguariensis): a comprehensive review on chemistry, health implications, and technological considerations. J Food Sci 2007; 72: 138–51. doi: 10.1111/j.1750-3841.2007.00535.x


28.
Oliveira DM, Freitas HS, Souza MF, Arçari DP, Ribeiro ML, Carvalho P O, et al. Yerba Maté (Ilex paraguariensis) aqueous extract decreases intestinal SGLT1 gene expression but does not affect other biochemical parameters in alloxan-diabetic Wistar rats. J Agric Food Chem 2008; 56: 10527–32.


29.
Michael N, Cillford Jose R, Ramirez M. Chorogeic acids and purine alkaloids contents of mate (Ilex paraguarinesis) leaf and beverage. Food Chem 1990; 35(1): 13–21. doi: 10.1016/0308-8146(90)90126-O


30.
Pomilio AB, Trajtemberg S, Vitale AA. High-performance capillary electrophoresis analysis of mate infusions prepared from stems and leaves of Ilex paraguariensis using automated micellar electrokinetic capillary chromatography. Phytochem Anal 2002; 13(4): 235–41. doi: 10.1002/pca.647


31.
Filip R, Sebastian T, Ferraro G, Anesini C. Effect of Ilex extracts and isolated compounds on peroxidase secretion of rat submandibular glands. Food Chem Toxicol 2007; 45(4): 649–55. doi: 10.1016/j.fct.2006.10.014


32.
Zaporozhets OA, Krushynska OA, Lipkovska NA, Barvinchenko VN. A new test method for the evaluation of total antioxidant activity of herbal products. J Agric Food Chem 2004; 52(1): 21–5. doi: 10.1021/jf0343480


33.
Martins F, Noso TM, Porto VB, Curiel A, Gambero A, Bastos DHM, et al. Maté tea inhibits in vitro pancreatic lipase activity and has hypolipidemic effect on high-fat diet-induced obese mice. Obesity 2009; 18: 42–7.


34.
Paganini Stein FL, Schmidt B, Furlong EB, Souza-Soares LA, Flores Soares MC, Cezar Vaz MR, et al. Vascular responses to extractable fractions of Ilex paraguariensis in rats fed standard and high-cholesterol diets. Biol Res Nurs 2005; 7: 146–56. doi: 10.1177/1099800405280521


35.
Mosimann AL, Wilhelm-Filho D, da Silva EL. Aqueous extract of Ilex paraguariensis attenuates the progression of atherosclerosis in cholesterol-fed rabbits. Biofactors 2005; 23: 1–12. doi: 10.1002/biof.5520260106


36.
Miranda DD, Arçari DP, Pedrazzoli J. Jr, Carvalho PdO, Cerutti SM, Bastos DHM, et al. Protective effects of mate tea (Ilex paraguariensis) on H2O2-induced DNA damage and DNA repair in mice. Mutagenesis 2008; 23: 261–5. doi: 10.1093/mutage/gen011


37.
Martins F, Suzan AJ, Cerutti SM, Arcari DP, Ribeiro ML, Markowicz Bastos DH, et al. Consumption of mate tea (Ilex paraguariensis) decreases the oxidation of unsaturated fatty acids in mouse liver. Br J Nutr 2009; 101: 527–32. doi: 10.1017/S000711450802504X


38.
Lanzetti M, Bezerra FS, Romana-Souza B, Brando-Lima AC, Goncalves Koatz VL, Porto LC, et al. Mate tea reduced acute lung inflammation in mice exposed to cigarette smoke. Nutrition 2008; 24: 375–81.


39.
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. Arch Biochem Biophys 2008;.476: 178–85. doi: 10.1016/j.abb.2008.02.019


40.
Gugliucci A. Antioxidant effects of Ilex paraguariensis: induction of decreased oxidability of human LDL in vivo. Biochem Biophys Res Commun 1996; 224: 338–44. doi: 10.1006/bbrc.1996.1030


41.
Bracesco N, Dell M, Rocha A, Behtash S, Menini T, Gugliucci A, et al. Antioxidant activity of a botanical extract preparation of Ilex paraguariensis: prevention of DNA double-strand breaks in Saccharomyces cerevisiae and human low-density lipoprotein oxidation. J Altern Complement Med 2003; 9: 379–87. doi: 10.1089/107555303765551606


42.
Menini T, Heck C, Schulze J, de Mejia E, Gugliucci A. Protective action of Ilex paraguariensis extract against free radical inactivation of paraoxonase-1 in high-density lipoprotein. Planta Med 2007; 73: 1141–7. doi: 10.1055/s-2007-981585


43.
Santos JC, Cotardo EMF, Briant MT, Piraee M, Gombero A, Ribeiro ML. Effects of Yerba maté, a plant extract formulation (‘YGD’) and resveratrol in 3T3-L1 adipogenesis. Molecules 2014; 19: 16909–24. doi: 10.3390/molecules191016909


44.
Hussein GM, Matsuda H, Nakamura S, Hamao M, Akiyama T, Tamura K, et al. Mate tea (Ilex paraguariensis) promotes satiety and body weight lowering in mice: involvement of glucagon-like peptide-1. Biol Pharm Bull 2011; 34: 1849–55.


45.
Pang GD, Lira FS, Rosa JC, Caris AV, Pinheiro F, Ribeiro EB, et al. Yerba mate extract (ilex paraguariensis) attenuates both central and peripheral inflammatory effects of diet-induced obesity in rats. J Nutr Biochem 2013; 24: 809–18. doi: 10.1016/j.jnutbio.2012.04.016


46.
Gosmann G, Barlette AG, Dhamer T, Arcari DP, Santos JC, de Camargo ER, et al. Phenolic compounds from mate (Ilex paraguariensis) inhibit adipogenesis in 3t3-l1 preadipocytes. Plant Foods Hum Nutr 2012; 67: 156–61.


47.
Arcari DP, Santos JC, Gambero A, Ferraz LF, Ribeiro ML. Modulatory effects of yerba mate (Ilex paraguariensis) on the pi3k-akt signaling pathway. Mol Nutr Food Res 2013; 57: 1882–5. doi: 10.1002/mnfr.201200834


48.
Arcari DP, Santos JC, Gambero A, Ribeiro ML. The in vitro and in vivo effects of yerba mate (Ilex paraguariensis) extract on adipogenesis. Food Chem 2013; 141: 809–15.


49.
Lima Nda S, Franco JG, Peixoto-Silva N, Maia LA, Kaezer A, Felzenszwalb I, et al. Ilex paraguariensis (yerba mate) improves endocrine and metabolic disorders in obese rats primed by early weaning. Eur J Nutr 2014; 53: 73–82. doi: 10.1007/s00394-013-0500-3


50.
Borges MC, Vinolo MA, Nakajima K, de Castro IA, Bastos DH, Borelli P, et al. The effect of mate tea (Ilex paraguariensis) on metabolic and inflammatory parameters in high-fat diet-fed wistar rats. Int J Food Sci Nutr 2013; 64: 561–9. doi: 10.3109/09637486.2012.759188


51.
Andersen T, Fogh J. Weight loss and delayed gastric emptying following a South American herbal preparation in overweight patients. J Hum Nutr Diet 2001; 14: 243–50. doi: 10.1046/j.1365-277X.2001.00290.x


52.
Kudo M, Yoshitomi H, Momoo M, Suguro S, Yamagishi Y, Gao M. Evaluation of the effects and mechanism of L-Citrulline on anti-obesity by appetite suppression in obese/diabetic KK-Ay mice and high-fat diet fed SD rats. Biol Pharm Bull 2017; 40: 524–30.


53.
Kudo M, Yamagishi Y, Suguro S, Nishihara M, Yoshitomi H, Hayashi M, et al. L-citrulline inhibits body weight gain and hepatic fat accumulation by improving lipid metabolism in a rat nonalcoholic fatty liver disease model. Food Sci Nutr 2021; 9: 4893–904.


54.
Kudo M, Yoshitomi H, Nishigaki T, Gao M. The effects of Morinda citrifolia (Noni) fruit juice on prevention of stoke by promoting production of nitric oxide through the brain of the spontaneously hypertensive stroke prone (SHRSP) rats. J Nutr Ther 2018; 7: 1–12. doi: 10.6000/1929-5634.2018.07.01.1


55.
Sun B, Hayashi M, Kudo M, Wu L, Qin L, Gao M, et al. Madecassoside inhibits body weight gain via modulating Sirt1-AMPK signaling pathway and activating genes related to thermogenesis. Front Endocrinol 2021; 9: 12: 627950. doi: 10.3389/fendo.2021.627950


56.
Hayashi M, Kudo M, Gao M. Plasmalogen inhibits body weight gain by activating brown adipose tissue and improving white adipose tissue metabolism. J Nutr Sci Vitaminol 2022; 68: 140–7.


57.
Kudo M, Hayashi M, Sun B, Wu L, Liu T, Gao M. Amycenone reduces excess body weight and attenuates hyperlipidemia by inhibiting lipogenesis and promoting lipolysis and fatty acid b-oxidation in KK-Ay obese diabetic mice. J Nutr Sci 2022; 11: e55. doi: 10.1017/jns.2022.43


58.
Kudo M, Hayashi M, Tian P, Liu D, Wu L, Li W, et al. YNCRG inhibited metabolic syndrome through appetite suppression and improved lipid metabolism in metabolic syndrome model rats. OBM Integr Complement Med 2020; 5(3).


59.
Yuan L, Tang P, Li HJ, Hu N, Zhong XY, Lin M, et al. Serum from Jiao-tai-Wan treated rats increases glucose consumption by 3T3-L1 adipocytes through AMPK pathway signaling. Biosci Rep 2019; 39: 1–10.


60.
Wang G, Wu B, Xu W, Jin X, Wang K, Wang H. The inhibitory effects of Juglanin on adipogenesis in 3T3-L1 adipocytes. Drug Des Devel Ther 2020; 14: 5349–57. doi: 10.2147/DDDT.S256504


61.
Yoshitomi H, Tsuru R, Li L. Zhou J, Kudo M, Liu T, et al. Cyclocarya paliurus extract activates insulin signaling via Sirtuin1 in C2C12 myotubes and decreases blood glucose level in mice with impaired insulin secretion. PLoS One 2017; 12(8): e0183988. doi: 10.1371/journal.pone.0183988


62.
Rimando AM, Perkins-Veazie PM, Determination of citrulline in watermelon rind. J Chromatogr A 2005; 1078: 196–200. doi: 10.1016/j.chroma.2005.05.009


63.
Li L, Yoshitomi H, Wei Y, Qin L, Zhou J, Xu T, et al. Tang-Nai-Kang alleviates pre-diabetes and metabolic disorders and induces a gene expression switch toward fatty acid oxidation in SHR.Cg-Leprcp/NDmcr Rats. PLoS One 2015; 10: e0122024. doi: 10.1371/journal.pone.0122024


64.
Okushin K, Tsutsumi T, Ikeuchi K, Kado A, Enooku K, Fujinaga H, et al. Heterozygous knock out of Bile salt export pump ameliorates liver steatosis in mice fed a high-fat diet. PLoS One 2020; 15(8): e0234750. doi: 10.1371/journal.pone.0234750


65.
Lee JS, Hyun IK, Seo HJ, Song D, Kim MY, Kang SS. Biotransformation of whey by Weissella cibaria suppresses 3T3-L1 adipocyte differentiation. Int J Dairy Sci 2021; 104: 3876–87. doi: 10.3168/jds.2020-19677


66.
Canbay A, Bechmann L, Gerken G. Lipid metabolism in the liver. Z Gastroenterol 2007; 45: 35–41.


67.
Ahn J, Lee H, Kim S, Ha T. Curcumin-induced suppression of adipogenic differentiation is accompanied by activation of Wnt/beta-catenin signaling. Am J Physiol Cell Physiol 2010; 298: 1510–6. doi: 10.1152/ajpcell.00369.2009


68.
Chen TX, Cheng XY, Wang Y, Yin W. Toosendanin inhibits adipogenesis by activating Wnt/beta-catenin signaling. Sci Rep 2018; 8: 4626.


69.
Choe WK, Kang BT, Kim SO. Water-extracted plum (Prunus salicina L. cv. Soldam) attenuates adipogenesis in murine 3T3-L1 adipocyte cells through the PI3K/Akt signaling pathway. Exp Ther Med 2018; 15: 1608–15.


70.
Mihaylova MM, Shaw RJ. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol 2011; 13: 1016–23. doi: 10.1038/ncb2329


71.
Zhang BB, Zhou GC, Li C. AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab 2009; 9: 407–16. doi: 10.1016/j.cmet.2009.03.012


72.
Porstmann T, Santos CR, Griffiths B, Cully M, Wu M, Leevers S, et al. SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell Metab 2008; 8: 224–36.


73.
Li Y, Xu S, Mihaylova MM, Zheng B, Hou X, Jiang B, et al. AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in diet-induced insulin-resistant mice. Cell Metab 2011; 13: 376–88. doi: 10.1016/j.cmet.2011.03.009


74.
Park YK, Obiang-Obounou BW, Lee KB, Choi JS, Jang BC. AZD1208, a pan-Pim kinase inhibitor, inhibits adipogenesis and induces lipolysis in 3T3-L1 adipocytes. J Cell Mol Med 2018; 22: 2488–97. doi: 10.1111/jcmm.13559


75.
Zhang J, Zhang SD, Wang P, Guo N, Wang W, Yao LP, et al. Pinolenic acid ameliorates oleic acid-induced lipogenesis and oxidative stress via AMPK/SIRT1 signaling pathway in HepG2 cells. Eur J Pharmacol 2019; 861: 172618. doi: 10.1016/j.ejphar.2019.172618


76.
Yang JY, Shi ZH, Ma W, Tao DQ, Liu S, Chen L, et al. Effect of Fuzi Lizhong decoction in reducing liver injury of rats with non-alcoholic fatty liver via activating AMPK and suppressing NF-kappaBp65 pathway. China J Chin Mater Med 2018; 43: 3176–83.


77.
Chu S, Narayan VP, Sung MK, Park T. Piperonal attenuates visceral adiposity in mice fed a high-fat diet: potential involvement of the adenylate cyclase-protein kinase A dependent pathway. Mol Nutr Food Res 2017; 61: 1601124. doi: 10.1002/mnfr.201601124


78.
Gormand A, Henriksson E, Strom K, Jense TE, Sakamoto K, Goransson O. Regulation of AMP-activated protein kinase by LKB1 and CaMKK in adipocytes. J Cell Biochem 2011; 112: 1364–75. doi: 10.1002/jcb.23053


79.
Lee YY, Kin M, Irfan M, Yuk HJ, Kim DS, Lee SE, et al. Ulmus parvifolia Jacq. Exhibits antiobesity properties and potentially induces browning of white adipose tissue. Evid Based Complementary Altern Med 2020; 9358563. doi: 10.1155/2020/9358563


80.
Mohamed-Ali V. Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-, in vivo. J Clin Endocrinol Metab 1997; 82: 4196–200.


81.
Haissaduerre M, Saucisse N, Cota D. Influence of mTOR in energy and metabolic homeostasis. Mol Cell Endocrinol 2014; 397: 67–77. doi: 10.1016/j.mce.2014.07.015


82.
Han YH, Kee JY, Park SH, Mun JG, Jeon HD, Park J, et al. Rubrofusarin-6-b-gentiobioside inhibits lipid accumulation and weight gain by regulating AMPK/mTOR signaling. Phytomedicine 2019; 62: 1–10. doi: 10.1016/j.phymed.2019.152952


83.
Malley CO, Pidgeon GP. The mTOR pathway in obesity driven gastrointestinal cancers: potential targets and clinical trials. BBA Clin 2015; 5: 29–40. doi: 10.1016/j.bbacli.2015.11.003


84.
Liu HW, Wei CC, Chen YJ, Chen YA, Chang SJ. Flavanol-rich lychee fruit extract alleviates diet-induced insulin resistance via suppressing mTOR/SREBP-1 mediated lipogenesis in liver and restoring insulin signaling in skeletal muscle. Mol Nutr Food Res 2016; 60: 2288–96. doi: 10.1002/mnfr.201501064


85.
Kim J, Yun JM, Kim MK, Kwon O, Cho B. Lactobacillus gasseri BNR17 supplementation reduces the visceral fat accumulation and waist circumference in obese adults: a randomized, double-blind, placebo-controlled trial. J Med Food 2018; 21: 454–61. doi: 10.1089/jmf.2017.3937


86.
Minami J, Iwabuchi N, Tanaka M, Yamauchi K, Xiao JZ, Abe F, et al. Effects of Bifidobacterium breve B-3 on body fat reductions in pre-obese adults: a randomized, double-blind, placebo-controlled trial. Biosci Microbiota Food Health 2018; 37: 67–75. doi: 10.12938/bmfh.18-001


87.
Hsu CL, Hou YH, Wanf CS, Lin SW, Jhou BY, Chen CC, et al. Antiobesity and uric acid-lowering effect of Lactobacullus plantarum GKM3 in high-fat-diet-induced obese rats. J Am Coll Nutr 2019; 38: 623–32. doi: 10.1080/07315724.2019.1571454


88.
Sztalryd C, Kraemer FB. Regulation of hormone-sensitive lipase in streptozotocin-induced diabetic rats. Metabolism 1995; 44: 1391–6. doi: 10.1016/0026-0495(95)90135-3


89.
Li CC, Yen CC, Fan CT, Chuang WT, Huang CS, Chen HW, et al. 14-Deoxy-11, 12-didehydroandrographolode suppresses adipogenesis of 3T3-L1 predipocytes by inhibiting CCAAT/enhancer-binding protein β activation and AMPK-mediated mitotic clonal expansion. Toxicol Appl Pharmacol 2018; 359: 82–90. doi: 10.1016/j.taap.2018.09.028
Published
2024-01-22
How to Cite
Kudo M., Gao M., Hayashi M., Kobayashi Y., Yang J., & Liu T. (2024). <em>Ilex paraguariensis</em&gt; A.St.-Hil. improves lipid metabolism in high-fat diet-fed obese rats and suppresses intracellular lipid accumulation in 3T3-L1 adipocytes via the AMPK-dependent and insulin signaling pathways. Food & Nutrition Research, 68. https://doi.org/10.29219/fnr.v68.10307
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Original Articles