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Inhibitory effects of Doenjang, Korean traditional fermented soybean paste, on oxidative stress and inflammation in adipose tissue of mice fed a high-fat diet

  • Nam, Ye Rim (Department of Food and Nutrition, Seoul National University) ;
  • Won, Sae Bom (Department of Food and Nutrition, Seoul National University) ;
  • Chung, Young-Shin (Department of Biotechnology, Hoseo University) ;
  • Kwak, Chung Shil (Institute on Aging, Seoul National University) ;
  • Kwon, Young Hye (Department of Food and Nutrition, Seoul National University)
  • Received : 2014.12.19
  • Accepted : 2015.02.16
  • Published : 2015.06.01

Abstract

BACKGROUND/OBJECTIVES: Doenjang, Korean traditional fermented soybean paste has been reported to have an anti-obesity effect. Because adipose tissue is considered a major source of inflammatory signals, we investigated the protective effects of Doenjang and steamed soybean on oxidative stress and inflammation in adipose tissue of diet-induced obese mice. MATERIALS/METHODS: Male C57BL/6J mice were fed a low fat diet (LF), a high-fat diet (HF), or a high-fat containing Doenjang diet (DJ) or a high-fat containing steamed soybean diet (SS) for 11 weeks. RESULTS: Mice fed a DJ diet showed significantly lower body and adipose tissue weights than those in the HF group. Although no significant differences in adipocyte size and number were observed among the HF diet-fed groups, consumption of Doenjang alleviated the incidence of crown-like structures in adipose tissue. Consistently, we observed significantly reduced mRNA levels of oxidative stress markers (heme oxygenase-1 and $p40^{phox}$), pro-inflammatory adipokines (tumor necrosis factor alpha and macrophage chemoattractant protein-1), macrophage markers (CD68 and CD11c), and a fibrosis marker (transforming growth factor beta 1) by Doenjang consumption. Gene expression of anti-inflammatory adipokine, adiponectin was significantly induced in the DJ group and the SS group compared to the HF group. The anti-oxidative stress and anti-inflammatory effects observed in mice fed an SS diet were not as effective as those in mice fed a DJ diet, suggesting that the bioactive compounds produced during fermentation and aging may be involved in the observed health-beneficial effects of Doenjang. CONCLUSIONS: Doenjang alleviated oxidative stress and restored the dysregulated expression of adipokine genes caused by excess adiposity. Therefore, Doenjang may ameliorate systemic inflammation and oxidative stress in obesity via inhibition of inflammatory signals of adipose tissue.

Keywords

References

  1. Ouchi N, Parker JL, Lugus JJ, Walsh K. Adipokines in inflammation and metabolic disease. Nat Rev Immunol 2011;11:85-97. https://doi.org/10.1038/nri2921
  2. Harwood HJ Jr. The adipocyte as an endocrine organ in the regulation of metabolic homeostasis. Neuropharmacology 2012;63:57-75. https://doi.org/10.1016/j.neuropharm.2011.12.010
  3. Maury E, Brichard SM. Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol 2010; 314:1-16. https://doi.org/10.1016/j.mce.2009.07.031
  4. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003;112:1796-808. https://doi.org/10.1172/JCI200319246
  5. Kim KY, Kim JK, Jeon JH, Yoon SR, Choi I, Yang Y. c-Jun N-terminal kinase is involved in the suppression of adiponectin expression by TNF-alpha in 3T3-L1 adipocytes. Biochem Biophys Res Commun 2005;327:460-7. https://doi.org/10.1016/j.bbrc.2004.12.026
  6. Maeda N, Takahashi M, Funahashi T, Kihara S, Nishizawa H, Kishida K, Nagaretani H, Matsuda M, Komuro R, Ouchi N, Kuriyama H, Hotta K, Nakamura T, Shimomura I, Matsuzawa Y. PPARgamma ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein. Diabetes 2001;50:2094-9. https://doi.org/10.2337/diabetes.50.9.2094
  7. Sun S, Ji Y, Kersten S, Qi L. Mechanisms of inflammatory responses in obese adipose tissue. Annu Rev Nutr 2012;32:261-86. https://doi.org/10.1146/annurev-nutr-071811-150623
  8. Kwon DY, Daily JW 3rd, Kim HJ, Park S. Antidiabetic effects of fermented soybean products on type 2 diabetes. Nutr Res 2010; 30:1-13. https://doi.org/10.1016/j.nutres.2009.11.004
  9. Chai C, Ju HK, Kim SC, Park JH, Lim J, Kwon SW, Lee J. Determination of bioactive compounds in fermented soybean products using GC/MS and further investigation of correlation of their bioactivities. J Chromatogr B Analyt Technol Biomed Life Sci 2012;880:42-9. https://doi.org/10.1016/j.jchromb.2011.11.013
  10. Chung SI, Rico CW, Kang MY. Comparative study on the hypoglycemic and antioxidative effects of fermented paste (doenjang) prepared from soybean and brown rice mixed with rice bran or red ginseng marc in mice fed with high fat diet. Nutrients 2014;6: 4610-24. https://doi.org/10.3390/nu6104610
  11. Jung KO, Park SY, Park KY. Longer aging time increases the anticancer and antimetastatic properties of doenjang. Nutrition 2006;22:539-45. https://doi.org/10.1016/j.nut.2005.11.007
  12. Park KY, Jung KO, Rhee SH, Choi YH. Antimutagenic effects of doenjang (Korean fermented soypaste) and its active compounds. Mutat Res 2003;523-524:43-53. https://doi.org/10.1016/S0027-5107(02)00320-2
  13. Gupta SC, Hevia D, Patchva S, Park B, Koh W, Aggarwal BB. Upsides and downsides of reactive oxygen species for cancer: the roles of reactive oxygen species in tumorigenesis, prevention, and therapy. Antioxid Redox Signal 2012;16:1295-322. https://doi.org/10.1089/ars.2011.4414
  14. Kwak CS, Park SC, Song KY. Doenjang, a fermented soybean paste, decreased visceral fat accumulation and adipocyte size in rats fed with high fat diet more effectively than nonfermented soybeans. J Med Food 2012;15:1-9. https://doi.org/10.1089/jmf.2010.1224
  15. Cha YS, Yang JA, Back HI, Kim SR, Kim MG, Jung SJ, Song WO, Chae SW. Visceral fat and body weight are reduced in overweight adults by the supplementation of Doenjang, a fermented soybean paste. Nutr Res Pract 2012;6:520-6. https://doi.org/10.4162/nrp.2012.6.6.520
  16. Fang N, Yu S, Badger TM. Comprehensive phytochemical profile of soy protein isolate. J Agric Food Chem 2004;52:4012-20. https://doi.org/10.1021/jf049842y
  17. Jeon S, Park YJ, Kwon YH. Genistein alleviates the development of nonalcoholic steatohepatitis in ApoE(-/-) mice fed a high-fat diet. Mol Nutr Food Res 2014;58:830-41. https://doi.org/10.1002/mnfr.201300112
  18. Ji G, Yang Q, Hao J, Guo L, Chen X, Hu J, Leng L, Jiang Z. Antiinflammatory effect of genistein on non-alcoholic steatohepatitis rats induced by high fat diet and its potential mechanisms. Int Immunopharmacol 2011;11:762-8. https://doi.org/10.1016/j.intimp.2011.01.036
  19. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007;87: 245-313. https://doi.org/10.1152/physrev.00044.2005
  20. Boschmann M, Engeli S, Adams F, Gorzelniak K, Franke G, Klaua S, Kreuzberg U, Luedtke S, Kettritz R, Sharma AM, Luft FC, Jordan J. Adipose tissue metabolism and CD11b expression on monocytes in obese hypertensives. Hypertension 2005;46:130-6. https://doi.org/10.1161/01.HYP.0000171477.63859.b2
  21. Li P, Lu M, Nguyen MT, Bae EJ, Chapman J, Feng D, Hawkins M, Pessin JE, Sears DD, Nguyen AK, Amidi A, Watkins SM, Nguyen U, Olefsky JM. Functional heterogeneity of CD11c-positive adipose tissue macrophages in diet-induced obese mice. J Biol Chem 2010; 285:15333-45. https://doi.org/10.1074/jbc.M110.100263
  22. Cawthorn WP, Sethi JK. TNF-alpha and adipocyte biology. FEBS Lett 2008;582:117-31. https://doi.org/10.1016/j.febslet.2007.11.051
  23. Bae CR, Kwon DY, Cha YS. Anti-obesity effects of traditional and standardized meju in high-fat diet-induced obese C57BL/6J mice. J Clin Biochem Nutr 2014;54:45-50. https://doi.org/10.3164/jcbn.13-52
  24. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004;114:1752-61. https://doi.org/10.1172/JCI21625
  25. Jiang F, Lim HK, Morris MJ, Prior L, Velkoska E, Wu X, Dusting GJ. Systemic upregulation of NADPH oxidase in diet-induced obesity in rats. Redox Rep 2011;16:223-9. https://doi.org/10.1179/174329211X13049558293713
  26. Nickelson KJ, Stromsdorfer KL, Pickering RT, Liu TW, Ortinau LC, Keating AF, Perfield JW 2nd. A comparison of inflammatory and oxidative stress markers in adipose tissue from weight-matched obese male and female mice. Exp Diabetes Res 2012;2012:859395.
  27. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006;86: 583-650. https://doi.org/10.1152/physrev.00011.2005
  28. Bouloumie A, Marumo T, Lafontan M, Busse R. Leptin induces oxidative stress in human endothelial cells. FASEB J 1999;13:1231-8. https://doi.org/10.1096/fasebj.13.10.1231
  29. Stojsavljevic S, Gomercic Palcic M, Virovic Jukic L, Smircic Duvnjak L, Duvnjak M. Adipokines and proinflammatory cytokines, the key mediators in the pathogenesis of nonalcoholic fatty liver disease. World J Gastroenterol 2014;20:18070-91. https://doi.org/10.3748/wjg.v20.i48.18070
  30. Paz-Filho G, Mastronardi C, Franco CB, Wang KB, Wong ML, Licinio J. Leptin: molecular mechanisms, systemic pro-inflammatory effects, and clinical implications. Arq Bras Endocrinol Metabol 2012;56: 597-607. https://doi.org/10.1590/S0004-27302012000900001
  31. Ouchi N, Walsh K. Adiponectin as an anti-inflammatory factor. Clin Chim Acta 2007;380:24-30. https://doi.org/10.1016/j.cca.2007.01.026
  32. Sun K, Tordjman J, Clement K, Scherer PE. Fibrosis and adipose tissue dysfunction. Cell Metab 2013;18:470-7. https://doi.org/10.1016/j.cmet.2013.06.016
  33. Leask A, Abraham DJ. TGF-beta signaling and the fibrotic response. FASEB J 2004;18:816-27. https://doi.org/10.1096/fj.03-1273rev
  34. Liu XJ, Yang L, Mao YQ, Wang Q, Huang MH, Wang YP, Wu HB. Effects of the tyrosine protein kinase inhibitor genistein on the proliferation, activation of cultured rat hepatic stellate cells. World J Gastroenterol 2002;8:739-45. https://doi.org/10.3748/wjg.v8.i4.739
  35. Shirakawa J, Fujii H, Ohnuma K, Sato K, Ito Y, Kaji M, Sakamoto E, Koganei M, Sasaki H, Nagashima Y, Amo K, Aoki K, Morimoto C, Takeda E, Terauchi Y. Diet-induced adipose tissue inflammation and liver steatosis are prevented by DPP-4 inhibition in diabetic mice. Diabetes 2011;60:1246-57. https://doi.org/10.2337/db10-1338
  36. Divoux A, Tordjman J, Lacasa D, Veyrie N, Hugol D, Aissat A, Basdevant A, Guerre-Millo M, Poitou C, Zucker JD, Bedossa P, Clement K. Fibrosis in human adipose tissue: composition, distribution, and link with lipid metabolism and fat mass loss. Diabetes 2010; 59:2817-25. https://doi.org/10.2337/db10-0585
  37. Nagaraju GP, Zafar SF, El-Rayes BF. Pleiotropic effects of genistein in metabolic, inflammatory, and malignant diseases. Nutr Rev 2013;71:562-72. https://doi.org/10.1111/nure.12044
  38. Omoni AO, Aluko RE. Soybean foods and their benefits: potential mechanisms of action. Nutr Rev 2005;63:272-83. https://doi.org/10.1111/j.1753-4887.2005.tb00141.x
  39. Korhonen H, Pihlanto A. Food-derived bioactive peptides--opportunities for designing future foods. Curr Pharm Des 2003;9:1297-308. https://doi.org/10.2174/1381612033454892
  40. Kwon DY, Hong SM, Ahn IS, Kim MJ, Yang HJ, Park S. Isoflavonoids and peptides from meju, long-term fermented soybeans, increase insulin sensitivity and exert insulinotropic effects in vitro. Nutrition 2011;27:244-52. https://doi.org/10.1016/j.nut.2010.02.004

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