Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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High-Molecular-Weight Poly-Gamma-Glutamate Protects Against Hypertriglyceridemic Effects of a High-Fructose Diet in Rat

  • Received : 2012.11.20
  • Accepted : 2013.02.22
  • Published : 2013.06.28
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Abstract

We studied the effects of 2 different dosages of high-molecular-weight poly-${\gamma}$-glutamic acid (hm ${\gamma}$-PGA) derived from Bacillus subtilis chungkookjang on lipid metabolism in a high-fructose diet-induced hypertriglyceridemic animal model. For 4 weeks, rats were fed either AIN-93 diet (normal control, NC; n = 10) or modified AIN-93 diet in which cornstarch was substituted with 63% fructose (n = 30) to induce hypertriglyceridemia. After 4 weeks, the hypertriglyceridemic rats were treated with daily oral doses of 0 mg (hypertriglyceridemic control, HC), 2.5 mg (hypertriglyceridemic, low hm ${\gamma}$-PGA, HL), or 5 $mg{\cdot}kg{\cdot}bw^{-1}{\cdot}d^{-1}$ (hypertriglyceridemic, high hm ${\gamma}$-PGA, HH) hm ${\gamma}$-PGA for 4 weeks. The HL and HH groups exhibited significantly lower levels of serum triglyceride, total cholesterol, LDL cholesterol, and free fatty acids than the HC group. The administration of hm ${\gamma}$-PGA reduced serum ALT and AST levels. The activities of lipogenic enzymes such as hepatic malic enzyme and glucose-6-phosphate dehydrogenase as well as glucose-6-phosphate dehydrogenase mRNA expression were significantly decreased by hm ${\gamma}$-PGA administration (p < 0.05). These results indicate that hm ${\gamma}$-PGA has an anti-hypertriglyceridemic effect in high-fructose diet-induced hypertriglyceridemic rats.

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References

  1. Arner, P. 2003. The adipocyte in insulin resistance: Key molecules and the impact of the thiazolidinediones. Trends Endocrinol. Metab. 14: 137-145. https://doi.org/10.1016/S1043-2760(03)00024-9
  2. Austin, M. A., P. J. E. Hokanson, and K. L. Edwards. 1998. Hypertriglyceridemia as a cardiovascular risk factor. Am. J. Cardiol. 81(4, Supplement 1): 7B-12B. https://doi.org/10.1016/S0002-9149(98)00031-9
  3. Back, H. I., S. R. Kim, J. A. Yang, M. G. Kim, S. W. Chae, and Y. S. Cha. 2011. Effects of Chungkookjang supplementation on obesity and atherosclerotic indices in overweight/obese subjects: A 12-week, randomized, double-blind, placebo-controlled clinical trial. J. Med. Food 14: 532-537. https://doi.org/10.1089/jmf.2010.1199
  4. Bartus, M., M. Lomnicka, B. Lorkowska, M. Franczyk, R. B. Kostogrys, P. M. Pisulewski, and S. Ch opicki. 2005. Hypertriglyceridemia but not hypercholesterolemia induces endothelial dysfunction in the rat. Pharmcol. Rep. 57(Suppl): 127-137.
  5. Choi, H., S. Song, J. Kim, J. Chung, J. Yoon, H. Y. Paik, and Y. Song. 2012. High carbohydrate intake was inversely associated with high-density lipoprotein cholesterol among Korean adults. Nutr. Res. 32: 100-106. https://doi.org/10.1016/j.nutres.2011.12.013
  6. Deibert, P., D. Konig, A. Schmidt-Trucksaess, K. S. Zaenker, I. Frey, U. Landmann, and A. Berg. 2004. Weight loss without losing muscle mass in pre-obese and obese subjects induced by a high-soy-protein diet. Int. J. Obes. Relat. Metab. Disord. 28: 1349-1352. https://doi.org/10.1038/sj.ijo.0802765
  7. Desai, M., D. Gayle, J. Babu, and M.G. Ross. 2007. The timing of nutrient restriction during rat pregnancy/lactation alters metabolic syndrome phenotype. Am. J. Obstet. Gynecol. 196: 555.e1-55.e7. https://doi.org/10.1016/j.ajog.2006.11.036
  8. Folch, J., M. Lees, and G. H. Sloane Stanley. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226: 497-509.
  9. Franz, G. 1979. Metabolism of reserve polysaccharides in tubers of Orchis morio L. Planta Med. 36: 68-73. https://doi.org/10.1055/s-0028-1097242
  10. Friedewald, W. T., R. I. Levy, and D. S. Fredrickson. 1972. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin. Chem. 18: 499-502.
  11. Frisinghelli, A. and A. Mafrici. 2007. Regression or reduction in progression of atherosclerosis, and avoidance of coronary events, with lovastatin in patients with or at high risk of cardiovascular disease: A review. Clin. Drug Invest. 27: 591-604. https://doi.org/10.2165/00044011-200727090-00001
  12. Glock, G. E. and L. P. McLean. 1953. Further studies on the properties and assay of glucose 6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase of rat liver. Biochem. J. 55: 400-408. https://doi.org/10.1042/bj0550400
  13. Grefhorst, A., B. M. Elzinga, P. J. Voshol, T. Plosch, T. Kok, V. W. Bloks, et al. 2002. Stimulation of lipogenesis by pharmacological activation of the liver X receptor leads to production of large, triglyceride-rich very low density lipoprotein particles. J. Biol. Chem. 277: 34182-34190. https://doi.org/10.1074/jbc.M204887200
  14. Gupte, R. S., B. C. Floyd, M. Kozicky, S. George, Z. I. Ungvari, V. Neito, et al. 2009. Synergistic activation of glucose-6- phosphate dehydrogenase and NAD(P)H oxidase by Src kinase elevates superoxide in type 2 diabetic, Zucker fa/fa, rat liver. Free Radic. Biol. Med. 47: 219-228. https://doi.org/10.1016/j.freeradbiomed.2009.01.028
  15. Herzberg, G. R. and M. Rogerson. 1988. Hepatic fatty acid synthesis and triglyceride secretion in rats fed fructose-or glucose-based diets containing corn oil, tallow or marine oil. J. Nutr. 118: 1061-1067. https://doi.org/10.1093/jn/118.9.1061
  16. Iwai, K., N. Nakaya, Y. Kawasaki, and H. Matsue. 2002. Antioxidative functions of natto, a kind of fermented soybeans: Effect on LDL oxidation and lipid metabolism in cholesterolfed rats. J. Agric. Food Chem. 50: 3597-3601. https://doi.org/10.1021/jf0117199
  17. Jensen, M. D. 2006. Is visceral fat involved in the pathogenesis of the metabolic syndrome? Human model. Obesity (Silver Spring) 14(Suppl 1): 20S-24S. https://doi.org/10.1038/oby.2006.278
  18. Kim, M. H., M. K. Kim, B. Y. Choi, and Y. J. Shin. 2004. Prevalence of the metabolic syndrome and its association with cardiovascular diseases in Korea. J. Kor. Med. Sci. 19: 195-201. https://doi.org/10.3346/jkms.2004.19.2.195
  19. Kim, N. Y., E. J. Song, D. Y. Kwon, H. P. Kim, and M. Y. Heo. 2008. Antioxidant and antigenotoxic activities of Korean fermented soybean. Food Chem. Toxicol. 46: 1184-1189. https://doi.org/10.1016/j.fct.2007.12.003
  20. Kwon, D. Y., J. W. Daily 3rd, H. J. Kim, and S. Park. 2010. Antidiabetic effects of fermented soybean products on type 2 diabetes. Nutr. Res. 30: 1-13. https://doi.org/10.1016/j.nutres.2009.11.004
  21. Lam, T. K., A. Carpentier, G. F. Lewis, G. van de Werve, I. G. Fantus, and A. Giacca. 2003. Mechanisms of the free fatty acidinduced increase in hepatic glucose production. Am. J. Physiol. Endocrinol. Metab. 284: E863-E873. https://doi.org/10.1152/ajpendo.00033.2003
  22. Lim, K. H., J. H. Han, Y. S. Park, Y. S. Cho, K. D. Kang, W. J. Yuk, et al. 2012. Assessment of antidiabetogenic potential of fermented soybean extracts in streptozotocin-induced diabetic rat. Food Chem. Toxicol. 50: 3941-3948. https://doi.org/10.1016/j.fct.2012.08.036
  23. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265-275.
  24. Lucas, E. A., S. A. Lightfoot, L. J. Hammond, L. Devareddy, D. A. Khalil, B. P. Daggy, et al. 2004. Flaxseed reduces plasma cholesterol and atherosclerotic lesion formation in ovariectomized Golden Syrian hamsters. Atherosclerosis 173: 223-229. https://doi.org/10.1016/j.atherosclerosis.2003.12.032
  25. Maki, K. C., D. N. Butteiger, T. M. Rains, A. Lawless, M. S. Reeves, C. Schasteen, and E. S. Krul. 2010. Effects of soy protein on lipoprotein lipids and fecal bile acid excretion in men and women with moderate hypercholesterolemia. J. Clin. Lipidol. 4: 531-542. https://doi.org/10.1016/j.jacl.2010.09.001
  26. Manninen, V., L. Tenkanen, P. Koskinen, J. K. Huttunen, M. Manttari, O. P. Heinonen, and M. H. Frick. 1992. Joint effects of serum triglyceride and LDL cholesterol and HDL cholesterol concentrations on coronary heart disease risk in the Helsinki Heart Study. Implications for treatment. Circulation 85: 37-45. https://doi.org/10.1161/01.CIR.85.1.37
  27. Meckling, K. A., C. O'Sullivan, and D. Saari. 2004. Comparison of a low-fat diet to a low-carbohydrate diet on weight loss, body composition, and risk factors for diabetes and cardiovascular disease in free-living, overweight men and women. J. Clin. Endocrinol. Metab. 89: 2717-2723. https://doi.org/10.1210/jc.2003-031606
  28. Min, H. K., H. J. Kim, and H. C. Chang. 2008. Growthinhibitory effect of the extract of porphyran-Chungkookjang on cancer cell. J. Kor. Soc. Food Sci. Nutr. 37: 826-833. https://doi.org/10.3746/jkfn.2008.37.7.826
  29. Nakagawa, T., H. Hu, S. Zharikov, K. R. Tuttle, R. A. Short, O. Glushakova, et al. 2006. A causal role for uric acid in fructoseinduced metabolic syndrome. Am. J. Physiol. Renal Physiol. 290: F625-F631. https://doi.org/10.1152/ajprenal.00140.2005
  30. Oh, J. Y., Y. S. Hong, Y. A. Sung, and E. Barrett-Connor. 2004. Prevalence and factor analysis of metabolic syndrome in an urban Korean population. Diabetes Care 27: 2027-2032. https://doi.org/10.2337/diacare.27.8.2027
  31. Oka, K. and L. Chan. 2005. Inhibition and regression of atherosclerotic lesions. Acta Biochim. Pol. 52: 311-319.
  32. Onat, A., I. Sari, M. Yazici, G. Can, G. Hergenc, and G. S. Avci. 2006. Plasma triglycerides, an independent predictor of cardiovascular disease in men: A prospective study based on a population with prevalent metabolic syndrome. Int. J. Cardiol. 108: 89-95. https://doi.org/10.1016/j.ijcard.2005.06.056
  33. Park, C., J. C. Choi, Y. H. Choi, H. Nakamura, K. Shimanouchi, T. Horiuchi, et al. 2005. Synthesis of super-high-molecular-weight poly-$\gamma$-glutamic acid by Bacillus subtilis subsp. chungkookjang. J. Mol. Catal. B Enzym. 35: 128-133. https://doi.org/10.1016/j.molcatb.2005.06.007
  34. Park, J. H., J. C. Choi, M. H. Sung, J. H. Kang, and M. J. Chang. 2011. High molecular weight poly-gamma-glutamic acid regulates lipid metabolism in rats fed a high-fat diet and humans. J. Microbiol. Biotechnol. 21: 766-775. https://doi.org/10.4014/jmb.1104.04047
  35. Park, S. S., Y. S. Yoon, and S. W. Oh. 2011. Health-related quality of life in metabolic syndrome: The Korea National Health and Nutrition Examination Survey 2005. Diabetes Res. Clin. Pract. 91: 381-388. https://doi.org/10.1016/j.diabres.2010.11.010
  36. Shankar, A., P. Mitchell, E. Rochtchina, and J. J. Wang. 2007. The association between circulating white blood cell count, triglyceride level and cardiovascular and all-cause mortality: Population-based cohort study. Atherosclerosis 192: 177-183. https://doi.org/10.1016/j.atherosclerosis.2006.04.029
  37. Shih, I. L. and Y. T. Van. 2001. The production of poly-($\gamma$-glutamic acid) from microorganisms and its various applications. Bioresour. Technol. 79: 207-225. https://doi.org/10.1016/S0960-8524(01)00074-8
  38. Sung, M. H., C. Park, C. J. Kim, H. Poo, K. Soda, and M. Ashiuchi. 2005. Natural and edible biopolymer poly-gammaglutamic acid: Synthesis, production, and applications. Chem. Rec. 5: 352-366. https://doi.org/10.1002/tcr.20061
  39. Tanimoto, H., M. Mori, M. Motoki, K. Torii, M. Kadowaki, and T. Noguchi. 2001. Natto mucilage containing poly-gammaglutamic acid increases soluble calcium in the rat small intestine. Biosci. Biotechnol. Biochem. 65: 516-521. https://doi.org/10.1271/bbb.65.516
  40. Torres, N., I. Torre-Villalvazo, and A. R. Tovar. 2006. Regulation of lipid metabolism by soy protein and its implication in diseases mediated by lipid disorders. J. Nutr. Biochem. 17: 365-373. https://doi.org/10.1016/j.jnutbio.2005.11.005
  41. Ueno, T., J. Tremblay, J. Kunes, J. Zicha, Z. Dobesova, Z. Pausova, et al. 2004. Rat model of familial combined hyperlipidemia as a result of comparative mapping. Physiol. Genomics 17: 38-47. https://doi.org/10.1152/physiolgenomics.00043.2003
  42. Wise, E. M. and E. G. Ball. 1964. Malic enzyme and lipogenesis. Proc. Natl. Acad. Sci. USA 52: 1255-1263. https://doi.org/10.1073/pnas.52.5.1255

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