Brown alga Ecklonia cava polyphenol extract ameliorates hepatic lipogenesis, oxidative stress, and inflammation by activation of AMPK and SIRT1 in high-fat diet-induced obese mice

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 1, 2015, Pages 349-359

  Eo, Hyeyoon ^a   Jeon, You Jin ^b   Lee, Myoungsook ^c   Lim, Yunsook ^a  

^a Kyung Hee University   (South Korea)

^b Jeju National University   (South Korea)

^c Sungshin Women's University   (South Korea)

Author keywords

AMPK; Ecklonia cava polyphenol extract; hepatic lipid metabolism; inflammation; obesity; SIRT1

Indexed keywords

ALGAE; ANTIOXIDANTS; CHEMICAL ACTIVATION; MAMMALS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

AMPK; INFLAMMATION; LIPID METABOLISMS; OBESITY; POLYPHENOL EXTRACT; SIRT1;

NUTRITION;

ECKLONIA CAVA; MUS; PHAEOPHYCEAE;

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; POLYPHENOL; SIRT1 PROTEIN, MOUSE; SIRTUIN 1;

ADVERSE EFFECTS; ANIMAL; BROWN ALGA; C57BL MOUSE; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GENETICS; HUMAN; INFLAMMATION; LIPID DIET; LIPOGENESIS; LIVER; MALE; METABOLISM; MOUSE; MOUSE MUTANT; OBESITY; OXIDATIVE STRESS;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; DIET, HIGH-FAT; HUMANS; INFLAMMATION; LIPOGENESIS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; OBESITY; OXIDATIVE STRESS; PHAEOPHYTA; POLYPHENOLS; SIRTUIN 1;

EID: 84921025779     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf502830b     Document Type: Article

References (47)

1. Jang, W. S.; Choung, S. Y. Antiobesity effects of the ethanol extract of Laminaria japonica Areshoung in high-fat-diet-induced obese rat Evidence-Based Complement. Altern. Medicine: eCAM 2013, 492807
2. Voshol, P. J.; Rensen, P. C.; van Dijk, K. W.; Romijn, J. A.; Havekes, L. M. Effect of plasma triglyceride metabolism on lipid storage in adipose tissue: studies using genetically engineered mouse models Biochim. Biophys. Acta 2009, 1791, 479-485
3. Koo, S. H. Nonalcoholic fatty liver disease: molecular mechanisms for the hepatic steatosis Clin. Mol. Hepatol. 2013, 19, 210-215
4. Tessari, P.; Coracina, A.; Cosma, A.; Tiengo, A. Hepatic lipid metabolism and non-alcoholic fatty liver disease Nutr., Metab., Cardiovasc. Dis. 2009, 19, 291-302
5. Viollet, B.; Guigas, B.; Leclerc, J.; Hebrard, S.; Lantier, L.; Mounier, R.; Andreelli, F.; Foretz, M. AMP-activated protein kinase in the regulation of hepatic energy metabolism: from physiology to therapeutic perspectives Acta Physiol. 2009, 196, 81-98
6. Hardie, D. G. Sensing of energy and nutrients by AMP-activated protein kinase Am. J. Clin. Nutr. 2011, 93, 891S-896S
7. Li, X. SIRT1 and energy metabolism Acta Biochim. Biophys. Sinica 2013, 45, 51-60
8. Colak, Y.; Ozturk, O.; Senates, E.; Tuncer, I.; Yorulmaz, E.; Adali, G.; Doganay, L.; Enc, F. Y. SIRT1 as a potential therapeutic target for treatment of nonalcoholic fatty liver disease Med. Sci. Monit.: Int. Med. J. Exp. Clin. Res. 2011, 17, HY5-HY9
9. Purushotham, A.; Schug, T. T.; Xu, Q.; Surapureddi, S.; Guo, X.; Li, X. Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation Cell Metab. 2009, 9, 327-338
10. Li, X.; Zhang, S.; Blander, G.; Tse, J. G.; Krieger, M.; Guarente, L. SIRT1 deacetylates and positively regulates the nuclear receptor LXR Mol. Cell 2007, 28, 91-106
11. Walker, A. K.; Yang, F.; Jiang, K.; Ji, J. Y.; Watts, J. L.; Purushotham, A.; Boss, O.; Hirsch, M. L.; Ribich, S.; Smith, J. J.; Israelian, K.; Westphal, C. H.; Rodgers, J. T.; Shioda, T.; Elson, S. L.; Mulligan, P.; Najafi-Shoushtari, H.; Black, J. C.; Thakur, J. K.; Kadyk, L. C.; Whetstine, J. R.; Mostoslavsky, R.; Puigserver, P.; Li, X.; Dyson, N. J.; Hart, A. C.; Naar, A. M. Conserved role of SIRT1 orthologs in fasting-dependent inhibition of the lipid/cholesterol regulator SREBP Genes Dev. 2010, 24, 1403-1417
12. Ponugoti, B.; Kim, D. H.; Xiao, Z.; Smith, Z.; Miao, J.; Zang, M.; Wu, S. Y.; Chiang, C. M.; Veenstra, T. D.; Kemper, J. K. SIRT1 deacetylates and inhibits SREBP-1C activity in regulation of hepatic lipid metabolism J. Biol. Chem. 2010, 285, 33959-33970
13. Ruderman, N. B.; Xu, X. J.; Nelson, L.; Cacicedo, J. M.; Saha, A. K.; Lan, F.; Ido, Y. AMPK and SIRT1: a long-standing partnership? Am. J. Physiol. Endocrinol. Metab. 2010, 298, E751-E760
14. Shen, Z.; Liang, X.; Rogers, C. Q.; Rideout, D.; You, M. Involvement of adiponectin-SIRT1-AMPK signaling in the protective action of rosiglitazone against alcoholic fatty liver in mice Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298, G364-G374
15. Li, Y.; Qian, Z. J.; Ryu, B.; Lee, S. H.; Kim, M. M.; Kim, S. K. Chemical components and its antioxidant properties in vitro: an edible marine brown alga, Ecklonia cava Bioorg. Med. Chem. 2009, 17, 1963-1973
16. Jung, W. K.; Ahn, Y. W.; Lee, S. H.; Choi, Y. H.; Kim, S. K.; Yea, S. S.; Choi, I.; Park, S. G.; Seo, S. K.; Lee, S. W.; Choi, I. W. Ecklonia cava ethanolic extracts inhibit lipopolysaccharide-induced cyclooxygenase-2 and inducible nitric oxide synthase expression in BV2 microglia via the MAP kinase and NF-kappaB pathways Food Chem. Toxicol. 2009, 47, 410-417
17. Park, S. J.; Kim, Y. T.; Jeon, Y. J. Antioxidant dieckol downregulates the Rac1/ROS signaling pathway and inhibits Wiskott-Aldrich syndrome protein (WASP)-family verprolin-homologous protein 2 (WAVE2)-mediated invasive migration of B16 mouse melanoma cells Mol. Cells 2012, 33, 363-369
18. Kim, T. H.; Ku, S. K.; Bae, J. S. Antithrombotic and profibrinolytic activities of eckol and dieckol J. Cell. Biochem. 2012, 113, 2877-2883
19. Ko, S. C.; Lee, M.; Lee, J. H.; Lee, S. H.; Lim, Y.; Jeon, Y. J. Dieckol, a phlorotannin isolated from a brown seaweed, Ecklonia cava, inhibits adipogenesis through AMP-activated protein kinase (AMPK) activation in 3T3-L1 preadipocytes Environ. Toxicol. Pharmacol. 2013, 36, 1253-1260
20. Kang, M. C.; Ahn, G.; Yang, X.; Kim, K. N.; Kang, S. M.; Lee, S. H.; Ko, S. C.; Ko, J. Y.; Kim, D.; Kim, Y. T.; Jee, Y.; Park, S. J.; Jeon, Y. J. Hepatoprotective effects of dieckol-rich phlorotannins from Ecklonia cava, a brown seaweed, against ethanol induced liver damage in BALB/c mice Food Chem. Toxicol. 2012, 50, 1986-1991
21. Kim, S. Y.; Kim, E. A.; Kang, M. C.; Lee, J. H.; Yang, H. W.; Lee, J. S.; Lim, T. I.; Jeon, Y. J. Polyphenol-rich fraction from Ecklonia cava (a brown alga) processing by-product reduces LPS-induced inflammation in vitro and in vivo in a zebrafish model Algae 2014, 29, 165-174
22. Lee, J. H.; Ko, J. Y.; Oh, J. Y.; Kim, C. Y.; Lee, H. J.; Kim, J.; Jeon, Y. J. Preparative isolation and purification of phlorotannins from Ecklonia cava using centrifugal partition chromatography by one-step Food Chem. 2014, 158, 433-437
23. Zhao, G.; Souers, A. J.; Voorbach, M.; Falls, H. D.; Droz, B.; Brodjian, S.; Lau, Y. Y.; Iyengar, R. R.; Gao, J.; Judd, A. S.; Wagaw, S. H.; Ravn, M. M.; Engstrom, K. M.; Lynch, J. K.; Mulhern, M. M.; Freeman, J.; Dayton, B. D.; Wang, X.; Grihalde, N.; Fry, D.; Beno, D. W.; Marsh, K. C.; Su, Z.; Diaz, G. J.; Collins, C. A.; Sham, H.; Reilly, R. M.; Brune, M. E.; Kym, P. R. Validation of diacyl glycerolacyltransferase I as a novel target for the treatment of obesity and dyslipidemia using a potent and selective small molecule inhibitor J. Med. Chem. 2008, 51, 380-383
24. Al-Hamodi, Z.; Al-Habori, M.; Al-Meeri, A.; Saif-Ali, R. Association of adipokines, leptin/adiponectin ratio and C-reactive protein with obesity and type 2 diabetes mellitus Diabetol. Metab. Syndrome 2014, 6, 99
25. Klop, B.; Elte, J. W.; Cabezas, M. C. Dyslipidemia in obesity: mechanisms and potential targets Nutrients 2013, 5, 1218-1240
26. Lee, S. H.; Min, K. H.; Han, J. S.; Lee, D. H.; Park, D. B.; Jung, W. K.; Park, P. J.; Jeon, B. T.; Kim, S. K.; Jeon, Y. J. Effects of brown alga, Ecklonia cava on glucose and lipid metabolism in C57BL/KsJ-db/db mice, a model of type 2 diabetes mellitus Food Chem. Toxicol. 2012, 50, 575-582
27. Gaemers, I. C.; Stallen, J. M.; Kunne, C.; Wallner, C.; van Werven, J.; Nederveen, A.; Lamers, W. H. Lipotoxicity and steatohepatitis in an overfed mouse model for non-alcoholic fatty liver disease Biochim. Biophys. Acta 2011, 1812, 447-458
28. Trauner, M.; Arrese, M.; Wagner, M. Fatty liver and lipotoxicity Biochim. Biophys. Acta 2010, 1801, 299-310
29. Liao, C. C.; Ou, T. T.; Wu, C. H.; Wang, C. J. Prevention of diet-induced hyperlipidemia and obesity by caffeic acid in C57BL/6 mice through regulation of hepatic lipogenesis gene expression J. Agric. Food Chem. 2013, 61, 11082-11088
30. Kim, S.; Jin, Y.; Choi, Y.; Park, T. Resveratrol exerts anti-obesity effects via mechanisms involving down-regulation of adipogenic and inflammatory processes in mice Biochem. Pharmacol. 2011, 81, 1343-1351
31. Shimano, H. Sterol regulatory element-binding proteins (SREBPs): transcriptional regulators of lipid synthetic genes Prog. Lipid Res. 2001, 40, 439-452
32. Kohjima, M.; Higuchi, N.; Kato, M.; Kotoh, K.; Yoshimoto, T.; Fujino, T.; Yada, M.; Yada, R.; Harada, N.; Enjoji, M.; Takayanagi, R.; Nakamuta, M. SREBP-1c, regulated by the insulin and AMPK signaling pathways, plays a role in nonalcoholic fatty liver disease Int. J. Mol. Med. 2008, 21, 507-511
33. Horton, J. D. Sterol regulatory element-binding proteins: transcriptional activators of lipid synthesis Biochem. Soc. Trans. 2002, 30, 1091-1095
34. Um, M. Y.; Hwang, K. H.; Ahn, J.; Ha, T. Y. Curcumin attenuates diet-induced hepatic steatosis by activating AMP-activated protein kinase Basic Clin. Pharmacol. Toxicol. 2013, 113, 152-157
35. Viollet, B.; Foretz, M.; Guigas, B.; Horman, S.; Dentin, R.; Bertrand, L.; Hue, L.; Andreelli, F. Activation of AMP-activated protein kinase in the liver: a new strategy for the management of metabolic hepatic disorders J. Physiol. 2006, 574, 41-53
36. Gower, B. A.; Nagy, T. R.; Blaylock, M. L.; Wang, C.; Nyman, L. Estradiol may limit lipid oxidation via Cpt 1 expression and hormonal mechanisms Obes. Res. 2002, 10, 167-172
37. Hou, X.; Xu, S.; Maitland-Toolan, K. A.; Sato, K.; Jiang, B.; Ido, Y.; Lan, F.; Walsh, K.; Wierzbicki, M.; Verbeuren, T. J.; Cohen, R. A.; Zang, M. SIRT1 regulates hepatocyte lipid metabolism through activating AMP-activated protein kinase J. Biol. Chem. 2008, 283, 20015-20026
38. Salminen, A.; Hyttinen, J. M.; Kaarniranta, K. AMP-activated protein kinase inhibits NF-kappaB signaling and inflammation: impact on healthspan and lifespan J. Mol. Med. 2011, 89, 667-676
39. Cohen, H. Y.; Miller, C.; Bitterman, K. J.; Wall, N. R.; Hekking, B.; Kessler, B.; Howitz, K. T.; Gorospe, M.; de Cabo, R.; Sinclair, D. A. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase Science 2004, 305, 390-392
40. Puigserver, P. Tissue-specific regulation of metabolic pathways through the transcriptional coactivator PGC1-alpha Int. J. Obes. 2005, 29 (Suppl. 1) S5-S9
41. Vachharajani, V.; Granger, D. N. Adipose tissue: a motor for the inflammation associated with obesity IUBMB Life 2009, 61, 424-430
42. Itabe, H. Oxidized low-density lipoprotein as a biomarker of in vivo oxidative stress: from atherosclerosis to periodontitis J. Clin. Biochem. Nutr. 2012, 51, 1-8
43. Chirico, S.; Smith, C.; Marchant, C.; Mitchinson, M. J.; Halliwell, B. Lipid peroxidation in hyperlipidaemic patients. A study of plasma using an HPLC-based thiobarbituric acid test Free Radical Res. Commun. 1993, 19, 51-57
44. Serafini-Cessi, F.; Cessi, C. Thiobarbituric acid test as an index of phospholipid peroxidation Sperimentale 1968, 118, 371-378
45. Ma, Y. Y.; Li, L.; Yu, C. H.; Shen, Z.; Chen, L. H.; Li, Y. M. Effects of probiotics on nonalcoholic fatty liver disease: a meta-analysis World J. Gastroenterol. 2013, 19, 6911-6918
46. 2-induced oxidative stress in murine hippocampal HT22 cells Environ. Toxicol. Pharmacol. 2012, 34, 96-105
47. Lim, H. H.; Yang, S. J.; Kim, Y.; Lee, M.; Lim, Y. Combined treatment of mulberry leaf and fruit extract ameliorates obesity-related inflammation and oxidative stress in high fat diet-induced obese mice J. Med. Food 2013, 16, 673-680