Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
권호 표지
DOI QR코드

DOI QR Code

Gelidium amansii extract ameliorates obesity by down-regulating adipogenic transcription factors in diet-induced obese mice

  • Kang, Ji-Hye (Department of Food Science and Nutrition, Pusan National University) ;
  • Lee, Hyun-Ah (Department of Food Science and Nutrition, Pusan National University) ;
  • Kim, Hak-Ju (Seojin Biotech Co., Ltd.) ;
  • Han, Ji-Sook (Department of Food Science and Nutrition, Pusan National University)
  • Received : 2016.05.09
  • Accepted : 2016.10.25
  • Published : 2017.02.01
Download PDF
⟨ Previous Next ⟩

Abstract

BACKGROUND/OBJECTIVES: In this study, we investigated whether Gelidium amansii extract (GAE) ameliorates obesity in diet-induced obese (DIO) mice. MATERIALS/METHODS: The mice were maintained on a high-fat diet (HD) for 5 weeks to generate the DIO mouse model. And then mice fed HD plus 0.5% (GAE1), 1% (GAE2) or 2% (GAE3) for 8 weeks. RESULTS: After the experimental period, GAE-supplemented groups were significantly lower than the HD group in body weight gain and liver weight. GAE supplemented groups were significantly lower than the HD group in both epididymal and mesenteric adipose tissue mass. The plasma leptin level was significantly higher in the HD group than in GAE-supplemented groups. The leptin level of HD+GAE3 group was significantly lower than that of the HD+conjugated linoleic acid (CLA) group. In contrast, plasma adiponectin level of the HD group was significantly lower than those of HD+GAE2 and HD+GAE3 groups. The expression levels of adipogenic proteins such as fatty acid synthase, sterol regulatory element-binding protein-1c, peroxisome proliferator-activated receptor ${\gamma}$, and CCAAT/enhancer binding protein ${\alpha}$ in the GAE supplemented groups were significantly decreased than those in HD group, respectively. In addition, the expression levels of HD+GAE2 and HD+GAE3 groups are significantly decreased compared to those of HD+CLA group. On the contrary, the expression levels of hormone-sensitive lipase and phospho-AMP-activated protein kinase, proteins associated with lipolysis, were significantly increased in the GAE supplemented groups compared to those in the HD group. HD+GAE3 group showed the highest level among the GAE supplemented groups. CONCLUSIONS: These results suggested that GAE supplementation stimulated the expressions of lipid metabolic factors and reduced weight gain in HD-fed C57BL/6J obese mice.

Keywords

References

  1. Nieves JW, Komar L, Cosman F, Lindsay R. Calcium potentiates the effect of estrogen and calcitonin on bone mass: review and analysis. Am J Clin Nutr 1998;67:18-24. https://doi.org/10.1093/ajcn/67.1.18
  2. Kopelman PG. Obesity as a medical problem. Nature 2000;404:635-43. https://doi.org/10.1038/35007508
  3. Wang T, Wang Y, Kontani Y, Kobayashi Y, Sato Y, Mori N, Yamashita H. Evodiamine improves diet-induced obesity in a uncoupling protein-1-independent manner: involvement of antiadipogenic mechanism and extracellularly regulated kinase/mitogen-activated protein kinase signaling. Endocrinology 2008;149:358-66. https://doi.org/10.1210/en.2007-0467
  4. Choi H, Eo H, Park K, Jin M, Park EJ, Kim SH, Park JE, Kim S. A water-soluble extract from Cucurbita moschata shows anti-obesity effects by controlling lipid metabolism in a high fat diet-induced obesity mouse model. Biochem Biophys Res Commun 2007;359:419-25. https://doi.org/10.1016/j.bbrc.2007.05.107
  5. Giri S, Rattan R, Haq E, Khan M, Yasmin R, Won JS, Key L, Singh AK, Singh I. AICAR inhibits adipocyte differentiation in 3T3L1 and restores metabolic alterations in diet-induced obesity mice model. Nutr Metab (Lond) 2006;3:31. https://doi.org/10.1186/1743-7075-3-31
  6. Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM. Transcriptional regulation of adipogenesis. Genes Dev 2000;14:1293-307.
  7. Sztalryd C, Kraemer FB. Regulation of hormone-sensitive lipase in streptozotocin-induced diabetic rats. Metabolism 1995;44:1391-6. https://doi.org/10.1016/0026-0495(95)90135-3
  8. Lefterova MI, Lazar MA. New developments in adipogenesis. Trends Endocrinol Metab 2009;20:107-14. https://doi.org/10.1016/j.tem.2008.11.005
  9. Wasan KM, Looije NA. Emerging pharmacological approaches to the treatment of obesity. J Pharm Pharm Sci 2005;8:259-71.
  10. Lee YS, Cha BY, Saito K, Choi SS, Wang XX, Choi BK, Yonezawa T, Teruya T, Nagai K, Woo JT. Effects of a Citrus depressa Hayata (shiikuwasa) extract on obesity in high-fat diet-induced obese mice. Phytomedicine 2011;18:648-54. https://doi.org/10.1016/j.phymed.2010.11.005
  11. Hofbauer KG, Nicholson JR. Pharmacotherapy of obesity. Exp Clin Endocrinol Diabetes 2006;114:475-84. https://doi.org/10.1055/s-2006-924241
  12. Bray GA. Medical therapy for obesity. Mt Sinai J Med 2010;77:407-17. https://doi.org/10.1002/msj.20207
  13. Choi KM, Lee YS, Shin DM, Lee S, Yoo KS, Lee MK, Lee JH, Kim SY, Lee YM, Hong JT, Yun YP, Yoo HS. Green tomato extract attenuates high-fat-diet-induced obesity through activation of the AMPK pathway in C57BL/6 mice. J Nutr Biochem 2013;24:335-42. https://doi.org/10.1016/j.jnutbio.2012.06.018
  14. Kadam SU, Prabhasankar P. Marine foods as functional ingredients in bakery and pasta products. Food Res Int 2010;43:1975-80. https://doi.org/10.1016/j.foodres.2010.06.007
  15. Yan X, Nagata T, Fan X. Antioxidative activities in some common seaweeds. Plant Foods Hum Nutr 1998;52:253-62. https://doi.org/10.1023/A:1008007014659
  16. Fu YW, Hou WY, Yeh ST, Li CH, Chen JC. The immunostimulatory effects of hot-water extract of Gelidium amansii via immersion, injection and dietary administrations on white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Fish Shellfish Immunol 2007;22:673-85. https://doi.org/10.1016/j.fsi.2006.08.014
  17. Yuan H, Song J, Li X, Li N, Dai J. Immunomodulation and antitumor activity of kappa-carrageenan oligosaccharides. Cancer Lett 2006;243:228-34. https://doi.org/10.1016/j.canlet.2005.11.032
  18. Kang MC, Kang N, Kim SY, Lima IS, Ko SC, Kim YT, Kim YB, Jeung HD, Choi KS, Jeon YJ. Popular edible seaweed, Gelidium amansii prevents against diet-induced obesity. Food Chem Toxicol 2016;90:181-7. https://doi.org/10.1016/j.fct.2016.02.014
  19. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972;18:499-502.
  20. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957;226:497-509.
  21. Yamashita Y, Okabe M, Natsume M, Ashida H. Prevention mechanisms of glucose intolerance and obesity by cacao liquor procyanidin extract in high-fat diet-fed C57BL/6 mice. Arch Biochem Biophys 2012;527:95-104. https://doi.org/10.1016/j.abb.2012.03.018
  22. Lee J, Chae K, Ha J, Park BY, Lee HS, Jeong S, Kim MY, Yoon M. Regulation of obesity and lipid disorders by herbal extracts from Morus alba, Melissa officinalis, and Artemisia capillaris in high-fat diet-induced obese mice. J Ethnopharmacol 2008;115:263-70. https://doi.org/10.1016/j.jep.2007.09.029
  23. Seo MJ, Lee OH, Choi HS, Lee BY. Extract from edible red seaweed (Gelidium amansii) inhibits lipid accumulation and ROS production during differentiation in 3T3-L1 cells. Prev Nutr Food Sci 2012;17:129-35. https://doi.org/10.3746/pnf.2012.17.2.129
  24. Hokanson JE, Austin MA. Plasma triglyceride level is a risk factor for cardiovascular disease independent of high-density lipoprotein cholesterol level: a meta-analysis of population-based prospective studies. J Cardiovasc Risk 1996;3:213-9.
  25. Miller M, Stone NJ, Ballantyne C, Bittner V, Criqui MH, Ginsberg HN, Goldberg AC, Howard WJ, Jacobson MS, Kris-Etherton PM, Lennie TA, Levi M, Mazzone T, Pennathur S; American Heart Association Clinical Lipidology, Thrombosis, and Prevention Committee of the Council on Nutrition, Physical Activity, and Metabolism; Council on Arteriosclerosis, Thrombosis and Vascular Biology; Council on Cardiovascular Nursing; Council on the Kidney in Cardiovascular Disease. Triglycerides and cardiovascular disease: a scientific statement from the American Heart Association. Circulation 2011;123:2292-333. https://doi.org/10.1161/CIR.0b013e3182160726
  26. den Boer M, Voshol PJ, Kuipers F, Havekes LM, Romijn JA. Hepatic steatosis: a mediator of the metabolic syndrome. Lessons from animal models. Arterioscler Thromb Vasc Biol 2004;24:644-9. https://doi.org/10.1161/01.ATV.0000116217.57583.6e
  27. Ferri M, Bin S, Vallini V, Fava F, Michelini E, Roda A, Minnucci G, Bucchi G, Tassoni A. Recovery of polyphenols from red grape pomace and assessment of their antioxidant and anti-cholesterol activities. N Biotechnol 2016;33:338-44. https://doi.org/10.1016/j.nbt.2015.12.004
  28. He ML, Wang Y, You JS, Mir PS, McAllister TA. Effect of a seaweed extract on fatty acid accumulation and glycerol-3-phosphate dehydrogenase activity in 3T3-L1 adipocytes. Lipids 2009;44:125-32. https://doi.org/10.1007/s11745-008-3256-4
  29. Korner A, Bluher S, Kapellen T, Garten A, Klammt J, Kratzsch J, Kiess W. Obesity in childhood and adolescence: a review in the interface between adipocyte physiology and clinical challenges. Hormones (Athens) 2005;4:189-99. https://doi.org/10.14310/horm.2002.11158
  30. Staiger H, Tschritter O, Machann J, Thamer C, Fritsche A, Maerker E, Schick F, Haring HU, Stumvoll M. Relationship of serum adiponectin and leptin concentrations with body fat distribution in humans. Obes Res 2003;11:368-72. https://doi.org/10.1038/oby.2003.48
  31. Jequier E. Leptin signaling, adiposity, and energy balance. Ann N Y Acad Sci 2002;967:379-88.
  32. Lee Y, Wang MY, Kakuma T, Wang ZW, Babcock E, McCorkle K, Higa M, Zhou YT, Unger RH. Liporegulation in diet-induced obesity. The antisteatotic role of hyperleptinemia. J Biol Chem 2001;276:5629-35. https://doi.org/10.1074/jbc.M008553200
  33. Wu X, Motoshima H, Mahadev K, Stalker TJ, Scalia R, Goldstein BJ. Involvement of AMP-activated protein kinase in glucose uptake stimulated by the globular domain of adiponectin in primary rat adipocytes. Diabetes 2003;52:1355-63. https://doi.org/10.2337/diabetes.52.6.1355
  34. Hu E, Liang P, Spiegelman BM. AdipoQ is a novel adipose-specific gene dysregulated in obesity. J Biol Chem 1996;271:10697-703. https://doi.org/10.1074/jbc.271.18.10697
  35. Siegrist M, Rank M, Wolfarth B, Langhof H, Haller B, Koenig W, Halle M. Leptin, adiponectin, and short-term and long-term weight loss after a lifestyle intervention in obese children. Nutrition 2013;29:851-7. https://doi.org/10.1016/j.nut.2012.12.011
  36. Bruun JM, Lihn AS, Verdich C, Pedersen SB, Toubro S, Astrup A, Richelsen B. Regulation of adiponectin by adipose tissue-derived cytokines: in vivo and in vitro investigations in humans. Am J Physiol Endocrinol Metab 2003;285:E527-33. https://doi.org/10.1152/ajpendo.00110.2003
  37. Park J, Rho HK, Kim KH, Choe SS, Lee YS, Kim JB. Overexpression of glucose-6-phosphate dehydrogenase is associated with lipid dysregulation and insulin resistance in obesity. Mol Cell Biol 2005;25:5146-57. https://doi.org/10.1128/MCB.25.12.5146-5157.2005
  38. Schoonjans K, Staels B, Auwerx J. The peroxisome proliferator activated receptors (PPARS) and their effects on lipid metabolism and adipocyte differentiation. Biochim Biophys Acta 1996;1302:93-109. https://doi.org/10.1016/0005-2760(96)00066-5
  39. Rosen ED, Hsu CH, Wang X, Sakai S, Freeman MW, Gonzalez FJ, Spiegelman BM. C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway. Genes Dev 2002;16:22-6. https://doi.org/10.1101/gad.948702
  40. Kamei R, Kitagawa Y, Kadokura M, Hattori F, Hazeki O, Ebina Y, Nishihara T, Oikawa S. Shikonin stimulates glucose uptake in 3T3-L1 adipocytes via an insulin-independent tyrosine kinase pathway. Biochem Biophys Res Commun 2002;292:642-51. https://doi.org/10.1006/bbrc.2002.6714
  41. Kim JB, Wright HM, Wright M, Spiegelman BM. ADD1/SREBP1 activates PPARgamma through the production of endogenous ligand. Proc Natl Acad Sci U S A 1998;95:4333-7. https://doi.org/10.1073/pnas.95.8.4333
  42. Evans RM, Barish GD, Wang YX. PPARs and the complex journey to obesity. Nat Med 2004;10:355-61. https://doi.org/10.1038/nm1025
  43. Wang S, Moustaid-Moussa N, Chen L, Mo H, Shastri A, Su R, Bapat P, Kwun I, Shen CL. Novel insights of dietary polyphenols and obesity. J Nutr Biochem 2014;25:1-18. https://doi.org/10.1016/j.jnutbio.2013.09.001
  44. Mohammed A, Al-Numair KS, Balakrishnan A. Docking studies on the interaction of flavonoids with fat mass and obesity associated protein. Pak J Pharm Sci 2015;28:1647-53.
  45. Zhang BB, Zhou G, Li C. AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab 2009;9:407-16. https://doi.org/10.1016/j.cmet.2009.03.012
  46. Jung HA, Jung HJ, Jeong HY, Kwon HJ, Ali MY, Choi JS. Phlorotannins isolated from the edible brown alga Ecklonia stolonifera exert anti-adipogenic activity on 3T3-L1 adipocytes by downregulating $C/EBP{\alpha}$ and $PPAR{\gamma}$. Fitoterapia 2014;92:260-9. https://doi.org/10.1016/j.fitote.2013.12.003
  47. Vingtdeux V, Chandakkar P, Zhao H, Davies P, Marambaud P. Small-molecule activators of AMP-activated protein kinase (AMPK), RSVA314 and RSVA405, inhibit adipogenesis. Mol Med 2011;17:1022-30.
  48. Hardie DG. AMPK: a key regulator of energy balance in the single cell and the whole organism. Int J Obes 2008;32 Suppl 4:S7-12. https://doi.org/10.1038/ijo.2008.116
  49. Watt MJ, Holmes AG, Pinnamaneni SK, Garnham AP, Steinberg GR, Kemp BE, Febbraio MA. Regulation of HSL serine phosphorylation in skeletal muscle and adipose tissue. Am J Physiol Endocrinol Metab 2006;290:E500-8. https://doi.org/10.1152/ajpendo.00361.2005
  50. Bezaire V, Mairal A, Ribet C, Lefort C, Girousse A, Jocken J, Laurencikiene J, Anesia R, Rodriguez AM, Ryden M, Stenson BM, Dani C, Ailhaud G, Arner P, Langin D. Contribution of adipose triglyceride lipase and hormone-sensitive lipase to lipolysis in hMADS adipocytes. J Biol Chem 2009;284:18282-91. https://doi.org/10.1074/jbc.M109.008631
  51. Son Y, Nam JS, Jang MK, Jung IA, Cho SI, Jung MH. Antiobesity activity of Vigna nakashimae extract in high-fat diet-induced obesity. Biosci Biotechnol Biochem 2013;77:332-8. https://doi.org/10.1271/bbb.120755

Cited by

  1. Gelidium amansii Extract, a Potent α-glucosidase and α-amylase Inhibitor, Alleviates Postprandial Hyperglycemia in Diabetic Mice vol.27, pp.9, 2017, https://doi.org/10.5352/jls.2017.27.9.1052
  2. Anti-inflammatory effects of Agar free-Gelidium amansii (GA) extracts in high-fat diet-induced obese mice vol.12, pp.6, 2017, https://doi.org/10.4162/nrp.2018.12.6.479
  3. Anti-obesity effects of Spirulina platensis protein hydrolysate by modulating brain-liver axis in high-fat diet fed mice vol.14, pp.6, 2017, https://doi.org/10.1371/journal.pone.0218543
  4. Effects of Gelidium elegans on Weight and Fat Mass Reduction and Obesity Biomarkers in Overweight or Obese Adults: A Randomized Double-Blinded Study vol.11, pp.7, 2017, https://doi.org/10.3390/nu11071513
  5. The Anti-Obesity Effect of Polysaccharide-Rich Red Algae (Gelidium amansii) Hot-Water Extracts in High-Fat Diet-Induced Obese Hamsters vol.17, pp.9, 2017, https://doi.org/10.3390/md17090532
  6. Anti-Obesity Effects of Macroalgae vol.12, pp.8, 2017, https://doi.org/10.3390/nu12082378
  7. Modeling Diet‐Induced Metabolic Syndrome in Rodents vol.64, pp.22, 2020, https://doi.org/10.1002/mnfr.202000249
  8. Molecular Mechanisms of the Anti-obesity Properties of Agardhiella subulata in Mice Fed a High-Fat Diet vol.69, pp.16, 2017, https://doi.org/10.1021/acs.jafc.1c01117