Gelidium elegans regulates the AMPK-PRDM16-UCP-1 pathway and has a synergistic effect with orlistat on obesity-associated features in mice fed a high-fat diet

Nutrients

Volumn 9, Issue 4, 2017, Pages

  Choi, Jia ^a   Kim, Kui Jin ^a   Koh, Eun Jeong ^a   Lee, Boo Yong ^a  

^a CHA University   (South Korea)

Author keywords

Gelidium amansii; Gelidium elegans; High fat diet induced obese mice; Hyperglycemia; Obesity

Indexed keywords

ADENYLATE KINASE; ALGAL EXTRACT; GELIDIUM ELEGANS EXTRACT; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; METFORMIN; PR DOMAIN CONTAINING16; TETRAHYDROLIPSTATIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1; ANTIOBESITY AGENT; DNA BINDING PROTEIN; GLUCOSE BLOOD LEVEL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; LACTONE; PLANT EXTRACT; PRDM16 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; UCP1 PROTEIN, MOUSE;

ABDOMINAL FAT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMICAL ANALYSIS; CONTROLLED STUDY; GELIDIUM ELEGANS; GENE EXPRESSION; GENE REPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; HYPERGLYCEMIA; INSULIN BLOOD LEVEL; LIPID DIET; LIPOGENESIS; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; ORGAN WEIGHT; PROTEIN PHOSPHORYLATION; RED ALGA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBCUTANEOUS FAT; WEIGHT GAIN; WESTERN BLOTTING; WHITE ADIPOSE TISSUE; ANIMAL; BLOOD; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; ORGAN SIZE; SIGNAL TRANSDUCTION;

ADIPOSITY; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTI-OBESITY AGENTS; BLOOD GLUCOSE; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; GLUCOSE TOLERANCE TEST; INSULIN; LACTONES; MALE; MICE; MICE, INBRED ICR; OBESITY; ORGAN SIZE; PLANT EXTRACTS; RHODOPHYTA; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UNCOUPLING PROTEIN 1; WEIGHT GAIN;

EID: 85016980370     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu9040342     Document Type: Article

References (60)

1. World Health Organization. Obesity: Preventing and Managing the Global Epidemic;World Health Organization: Geneva, Switzerland, 2000.
2. Farmer, S.R. Regulation of ppargamma activity during adipogenesis. Int. J. Obes. 2005, 29 (Suppl. 1), S13-S16. [CrossRef] [PubMed]
3. Dandona, P.; Aljada, A.; Bandyopadhyay, A. Inflammation: The link between insulin resistance, obesity and diabetes. Trends Immunol. 2004, 25, 4-7. [CrossRef] [PubMed]
4. Dobbs, R.; Sawers, C.; Thompson, F.; Manyika, J.; Woetzel, J.R.; Child, P.; McKenna, S.; Spatharou, A. Overcoming Obesity: An Initial Economic Analysis; McKinsey Global Institute: Tamil Nadu, India, 2014.
5. Roberts, D.L.; Dive, C.; Renehan, A.G. Biological mechanisms linking obesity and cancer risk: New perspectives. Annu. Rev. Med. 2010, 61, 301-316. [CrossRef] [PubMed]
6. Lau, D.C.; Douketis, J.D.; Morrison, K.M.; Hramiak, I.M.; Sharma, A.M.; Ur, E. Obesity Canada Clinical Practice Guidelines Expert Panel. Can. Med. Assoc. J. 2007, 176, S1-S13. [CrossRef] [PubMed]
7. Pi-Sunyer, F.X.; Becker, D.M.; Bouchard, C.; Carleton, R.; Colditz, G.; Dietz, W.; Foreyt, J.; Garrison, R.; Grundy, S.; Hansen, B. Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults. Am. J. Clin. Nutr. 1998, 68, 899-917.
8. Heck, A.M.; Yanovski, J.A.; Calis, K.A. Orlistat, a new lipase inhibitor for the management of obesity. Pharmacotherapy 2000, 20, 270-279. [CrossRef] [PubMed]
9. Rossner, S.; Sjostrom, L.; Noack, R.; Meinders, E.; Noseda, G. Weight loss, weight maintenance, and improved cardiovascular risk factors after 2 years treatment with orlistat for obesity. Obes. Res. 2000, 8, 49-61. [CrossRef] [PubMed]
10. Heymsfield, S.B.; Segal, K.R.; Hauptman, J.; Lucas, C.P.; Boldrin, M.N.; Rissanen, A.; Wilding, J.P.; Sjöström, L. Effects of weight loss with orlistat on glucose tolerance and progression to type 2 diabetes in obese adults. Arch. Intern. Med. 2000, 160, 1321-1326. [CrossRef] [PubMed]
11. Kumanyika, S.K.; Obarzanek, E.; Stettler, N.; Bell, R.; Field, A.E.; Fortmann, S.P.; Franklin, B.A.; Gillman, M.W.; Lewis, C.E.; Poston, W.C., et al. Population-based prevention of obesity the need for comprehensive promotion of healthful eating, physical activity, and energy balance: A scientific statement from american heart association council on epidemiology and prevention, interdisciplinary committee for prevention (formerly the expert panel on population and prevention science). Circulation 2008, 118, 428-464. [PubMed]
12. Epstein, L.H.; Gordy, C.C.; Raynor, H.A.; Beddome, M.; Kilanowski, C.K.; Paluch, R. Increasing fruit and vegetable intake and decreasing fat and sugar intake in families at risk for childhood obesity. Obes. Res. 2001, 9, 171-178. [CrossRef] [PubMed]
13. Szkudelska, K.; Szkudelski, T. Resveratrol, obesity and diabetes. Eur. J. Pharmacol. 2010, 635, 1-8. [CrossRef] [PubMed]
14. Ejaz, A.; Wu, D.; Kwan, P.; Meydani, M. Curcumin inhibits adipogenesis in 3t3-l1 adipocytes and angiogenesis and obesity in c57/bl mice. J. Nutr. 2009, 139, 919-925. [CrossRef] [PubMed]
15. Blankson, H.; Stakkestad, J.A.; Fagertun, H.; Thom, E.; Wadstein, J.; Gudmundsen, O. Conjugated linoleic acid reduces body fat mass in overweight and obese humans. J. Nutr. 2000, 130, 2943-2948. [PubMed]
16. Ruzickova, J.; Rossmeisl, M.; Prazak, T.; Flachs, P.; Sponarova, J.; Vecka, M.; Tvrzicka, E.; Bryhn, M.; Kopecky, J. Omega-3 pufa of marine origin limit diet-induced obesity in mice by reducing cellularity of adipose tissue. Lipids 2004, 39, 1177-1185. [CrossRef] [PubMed]
17. Miyashita, K. The carotenoid fucoxanthin from brown seaweed affects obesity. Lipid Technol. 2009, 21, 186-190. [CrossRef]
18. Maeda, H.; Tsukui, T.; Sashima, T.; Miyashita, K. Seaweed carotenoid, fucoxanthin, as a multi-functional nutrient. Asia Pac. J. Clin. Nutr. 2008, 17, 196-199. [PubMed]
19. Kang, M.-C.; Kang, N.; Kim, S.-Y.; Lima, I.S.; Ko, S.-C.; Kim, Y.-T.; Kim, Y.-B.; Jeung, H.-D.; Choi, K.-S.; Jeon, Y.-J. Popular edible seaweed, gelidium amansii prevents against diet-induced obesity. Food Chem. Toxicol. 2016, 90, 181-187. [CrossRef] [PubMed]
20. Yang, T.-H.; Yao, H.-T.; Chiang, M.-T. Red algae (gelidium amansii) reduces adiposity via activation of lipolysis in rats with diabetes induced by streptozotocin-nicotinamide. J. Food Drug Anal. 2015, 23, 758-765. [CrossRef]
21. Seo, M.-J.; Lee, O.-H.; Choi, H.-S.; Lee, B.-Y. 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, 129-135. [CrossRef] [PubMed]
22. Choi, J.; Kim, K.-J.; Koh, E.-J.; Lee, B.-Y. Altered gelidium elegans extract-stimulated beige-like phenotype attenuates adipogenesis in 3t3-l1 cells. J. Food Nutr. Res. 2016, 4, 448-453.
23. Kim, K.-J.; Choi, J.; Lee, B.-Y. Evaluation of the genotoxicity of a Gelidium elegans extract in vitro and in vivo. J. Food Nutr. Res. 2016, 4, 653-657.
24. Wang, Z.; Oh, E.; Clapp, D.W.; Chernoff, J.; Thurmond, D.C. Inhibition or ablation of p21-activated kinase (pak1) disrupts glucose homeostatic mechanisms in vivo. J. Biol. Chem. 2011, 286, 41359-41367. [CrossRef] [PubMed]
25. Harlow, E.D.; Lane, D. Using Antibodies: A Laboratory Manual; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA, 1999.
26. Morelli, A.; Filippi, S.; Comeglio, P.; Sarchielli, E.; Chavalmane, A.K.; Vignozzi, L.; Fibbi, B.; Silvestrini, E.; Sandner, P.; Gacci, M., et al. Acute vardenafil administration improves bladder oxygenation in spontaneously hypertensive rats. J. Sex. Med. 2010, 7, 107-120. [CrossRef] [PubMed]
27. Dubuc, P.U. The development of obesity, hyperinsulinemia, and hyperglycemia in ob/ob mice. Metabolism 1976, 25, 1567-1574. [CrossRef]
28. Newcomer, J.W. Metabolic syndrome and mental illness. Am. J. Manag. Care 2007, 13, S170-S177. [PubMed]
29. European Diabetes Policy Group. A desktop guide to type 2 diabetes mellitus. In Diabet. Med.; 1999; Volume 16, pp. 716-730.
30. Hillier, T.A.; Pedula, K.L.; Schmidt, M.M.; Mullen, J.A.; Charles, M.-A.; Pettitt, D.J. Childhood obesity and metabolic imprinting the ongoing effects of maternal hyperglycemia. Diabetes Care 2007, 30, 2287-2292. [CrossRef] [PubMed]
31. Watkins, M.L.; Rasmussen, S.A.; Honein, M.A.; Botto, L.D.; Moore, C.A. Maternal obesity and risk for birth defects. Pediatrics 2003, 111, 1152-1158. [PubMed]
32. Arai, T.; Yamashita, S.; Hirano, K.-I.; Sakai, N.; Kotani, K.; Fujioka, S.; Nozaki, S.; Keno, Y.; Yamane, M.; Shinohara, E., et al. Increased plasma cholesteryl ester transfer protein in obese subjects. A possible mechanism for the reduction of serum hdl cholesterol levels in obesity. Arterioscler. Thromb. 1994, 14, 1129-1136. [CrossRef] [PubMed]
33. Hu, E.; Tontonoz, P.; Spiegelman, B.M. Transdifferentiation of myoblasts by the adipogenic transcription factors ppar gamma and c/ebp alpha. Proc. Natl. Acad. Sci. USA 1995, 92, 9856-9860. [CrossRef] [PubMed]
34. Laakso, M. Hyperglycemia and cardiovascular disease in type 2 diabetes. Diabetes 1999, 48, 937-942. [CrossRef] [PubMed]
35. Ikemoto, S.; Takahashi, M.; Tsunoda, N.; Maruyama, K.; Itakura, H.; Ezaki, O. High-fat diet-induced hyperglycemia and obesity in mice: Differential effects of dietary oils. Metabolism 1996, 45, 1539-1546. [CrossRef]
36. Nathan, D.M.; Davidson, M.B.; DeFronzo, R.A.; Heine, R.J.; Henry, R.R.; Pratley, R.; Zinman, B. Impaired fasting glucose and impaired glucose tolerance. Diabetes Care 2007, 30, 753-759. [CrossRef] [PubMed]
37. Yang, L.; Zhang, Y.; Wang, L.; Fan, F.; Zhu, L.; Li, Z.; Ruan, X.; Huang, H.; Wang, Z.; Huang, Z., et al. Amelioration of high fat diet induced liver lipogenesis and hepatic steatosis by interleukin-22. J. Hepatol. 2010, 53, 339-347. [CrossRef] [PubMed]
38. Carmiel-Haggai, M.; Cederbaum, A.I.; Nieto, N. A high-fat diet leads to the progression of non-alcoholic fatty liver disease in obese rats. FASEB J. 2005, 19, 136-138. [CrossRef] [PubMed]
39. Horton, J.D.; Goldstein, J.L.; Brown, M.S. Srebps: Activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Investig. 2002, 109, 1125-1131. [CrossRef] [PubMed]
40. Yahagi, N.; Shimano, H.; Hasty, A.H.; Matsuzaka, T.; Ide, T.; Yoshikawa, T.; Amemiya-Kudo, M.; Tomita, S.; Okazaki, H.; Tamura, Y., et al. Absence of sterol regulatory element-binding protein-1 (srebp-1) ameliorates fatty livers but not obesity or insulin resistance inlep ob/lep ob mice. J. Biol. Chem. 2002, 277, 19353-19357. [CrossRef] [PubMed]
41. Brown, M.S.; Goldstein, J.L. The srebp pathway: Regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 1997, 89, 331-340. [CrossRef]
42. Harris, C.A.; Haas, J.T.; Streeper, R.S.; Stone, S.J.; Kumari, M.; Yang, K.; Han, X.; Brownell, N.; Gross, R.W.; Zechner, R., et al. Dgat enzymes are required for triacylglycerol synthesis and lipid droplets in adipocytes. J. Lipid Res. 2011, 52, 657-667. [CrossRef] [PubMed]
43. Li, Y.; Xu, S.; Mihaylova, M.M.; Zheng, B.; Hou, X.; Jiang, B.; Park, O.; Luo, Z.; Lefai, E.; Shyy, J.Y.-J., et al. Ampk phosphorylates and inhibits srebp activity to attenuate hepatic steatosis and atherosclerosis in diet-induced insulin-resistant mice. Cell Metab. 2011, 13, 376-388. [CrossRef] [PubMed]
44. Hardie, D.G. Ampk—Sensing energy while talking to other signaling pathways. Cell Metab. 2014, 20, 939-952. [CrossRef] [PubMed]
45. Kajimura, S.; Seale, P.; Tomaru, T.; Erdjument-Bromage, H.; Cooper, M.P.; Ruas, J.L.; Chin, S.; Tempst, P.; Lazar, M.A.; Spiegelman, B.M. Regulation of the brown and white fat gene programs through a prdm16/ctbp transcriptional complex. Genes Dev. 2008, 22, 1397-1409. [CrossRef] [PubMed]
46. Kang, J.H.; Tsuyoshi, G.; Han, I.S.; Kawada, T.; Kim, Y.M.; Yu, R. Dietary capsaicin reduces obesity-induced insulin resistance and hepatic steatosis in obese mice fed a high-fat diet. Obesity 2010, 18, 780-787. [CrossRef] [PubMed]
47. Maeda, H.; Hosokawa, M.; Sashima, T.; Murakami-Funayama, K.; Miyashita, K. Anti-obesity and anti-diabetic effects of fucoxanthin on diet-induced obesity conditions in a murine model. Mol. Med. Rep. 2009, 2, 897-902. [CrossRef] [PubMed]
48. Jayaprakasam, B.; Olson, L.K.; Schutzki, R.E.; Tai, M.-H.; Nair, M.G. Amelioration of obesity and glucose intolerance in high-fat-fed c57bl/6 mice by anthocyanins and ursolic acid in cornelian cherry (cornus mas). J. Agric. Food Chem. 2006, 54, 243-248. [CrossRef] [PubMed]
49. Jeon, H.J.; Seo, M.J.; Choi, H.S.; Lee, O.H.; Lee, B.Y. Gelidium elegans, an edible red seaweed, and hesperidin inhibit lipid accumulation and production of reactive oxygen species and reactive nitrogen species in 3t3-l1 and raw264.7 cells. Phytother. Res. 2014, 28, 1701-1709. [CrossRef] [PubMed]
50. Gregor, M.F.; Hotamisligil, G.S. Inflammatory mechanisms in obesity. Annu. Rev. Immunol. 2011, 29, 415-445. [CrossRef] [PubMed]
51. Liu, H.-C.; Chang, C.-J.; Yang, T.-H.; Chiang, M.-T. Long-term feeding of red algae (Gelidium amansii) ameliorates glucose and lipid metabolism in a high fructose diet-impaired glucose tolerance rat model. J. Food Drug Anal. 2016. [CrossRef]
52. Zhang, H.; Zhang, S.; Jiang, C.; Li, Y.; Xu, G.; Xu, M.; Wang, X. Intermedin/adrenomedullin 2 polypeptide promotes adipose tissue browning and reduces high-fat diet-induced obesity and insulin resistance in mice. Int. J. Obes. 2016, 40, 852-860. [CrossRef] [PubMed]
53. Lin, J.; Yang, R.; Tarr, P.T.; Wu, P.-H.; Handschin, C.; Li, S.; Yang, W.; Pei, L.; Uldry, M.; Tontonoz, P., et al. Hyperlipidemic effects of dietary saturated fats mediated through pgc-1β coactivation of srebp. Cell 2005, 120, 261-273. [CrossRef] [PubMed]
54. Fernandez-Marcos, P.J.; Auwerx, J. Regulation of pgc-1alpha, a nodal regulator of mitochondrial biogenesis. Am. J. Clin. Nutr. 2011, 93, 884S-890S. [CrossRef] [PubMed]
55. Seale, P.; Kajimura, S.; Yang, W.; Chin, S.; Rohas, L.M.; Uldry, M.; Tavernier, G.; Langin, D.; Spiegelman, B.M. Transcriptional control of brown fat determination by prdm16. Cell Metab. 2007, 6, 38-54. [CrossRef] [PubMed]
56. Zelber-Sagi, S.; Kessler, A.; Brazowsky, E.; Webb, M.; Lurie, Y.; Santo, M.; Leshno, M.; Blendis, L.; Halpern, Z.; Oren, R. A double-blind randomized placebo-controlled trial of orlistat for the treatment of nonalcoholic fatty liver disease. Clin. Gastroenterol. Hepatol. 2006, 4, 639-644. [CrossRef] [PubMed]
57. Van Gaal, L.; Broom, J.; Enzi, G.; Toplak, H. Efficacy and tolerability of orlistat in the treatment of obesity: A 6-month dose-ranging study. Eur. J. Clin. Pharmacol. 1998, 54, 125-132. [CrossRef] [PubMed]
58. Kiortsis, D.; Filippatos, T.; Elisaf, M. The effects of orlistat on metabolic parameters and other cardiovascular risk factors. Diabetes Metab. 2005, 31, 15-22. [CrossRef]
59. Spiegelman, B.M.; Flier, J.S. Adipogenesis and obesity: Rounding out the big picture. Cell 1996, 87, 377-389. [CrossRef]
60. Hamilton, M.T.; Hamilton, D.G.; Zderic, T.W. Role of low energy expenditure and sitting in obesity, metabolic syndrome, type 2 diabetes, and cardiovascular disease. Diabetes 2007, 56, 2655-2667. [CrossRef] [PubMed]