Bacterial $\beta$-Glucan Exhibits Potent Hypoglycemic Activity via Decrease of Serum Lipids and Adiposity, and Increase of UCP mRNA Expression

  • HONG KYUNGHEE (Asan Institute for Life Science) ;
  • JANG KI-HYO (Department of Food and Nutrition, Samcheok National University) ;
  • LEE JAE-CHEOL (Department of Food and Nutrition, Samcheok National University) ;
  • KIM SOHYE (Health Medical Center, Seoul National University Bundang Hospital) ;
  • KIM MI-KYOUNG (DawMaJin Biotechnology Research Institute, DMJ Biotech Corp.) ;
  • LEE IN-YOUNG (DawMaJin Biotechnology Research Institute, DMJ Biotech Corp.) ;
  • KIM SANG-MOO (Faculty of Marine Bioscience and Technology, Kangnung National University) ;
  • LIM YOONG HO (Department of Molecular Biotechnology, Bio/Molecular Informatics Center, Konkuk University) ;
  • KANG SOON AH (Department of Molecular Biotechnology, Bio/Molecular Informatics Center, Konkuk University)
  • Published : 2005.08.01

Abstract

This study was undertaken to evaluate the effect of bacteria-derived $\beta$-glucan fiber on serum lipids, adiposity and uncoupling protein (UCP) expression in rats. In order to induce obesity, Sprague-Dawley weanling male rats were allowed free access to AIN-76A diet until 4 weeks of age, and fed high-fat diet (beef tallow, $40\%$ of calories as fat) for 6 weeks until 10 weeks of age. Rats were then fed with $0\%$ thigh- fat control group), $1\%$, or $5\%$ bacterial ~-glucan supplemented high-fat diets (w/w) for another 6 weeks. For comparison, normal control group was fed with AIN-76 diet $11.7\%$ fat). Supplementation with bacterial $\beta$-glucan resulted in a significant reduction of high-fat-induced white fat (i.e., visceral and peritoneal fat) development, adipocyte hypertrophy, and development of hyperinsulinemia and hyperleptinemia. Serum triglyceride, total cholesterol, and free fatty acid levels were greatly reduced, but, HDL-cholesterol concentrations were increased by bacterial $\beta$-glucan supplementation. Serum leptin level was lower in the $\beta$-glucan groups than in the high-fat group. The expression of UCPs (UCP1, UCP2, and UCP3) in brown adipose tissue (BAT) were significantly increased by $5\%$ bacterial $\beta$-glucan-containing diet. This study suggests that the anti-obesity effect of $5\%$ bacterial $\beta$-glucan is attributed to upregulation of UCPs and inefficient energy utilization.

Keywords

References

  1. Bobek, P., M. Hromadora, and J. Odin. 1995. Oyster mushroom (Pleurotus ostreatus) reduces the activity of 3-hydroxy-3-methylglutaryl . CoA reductase in rat liver microsomes. Experientia 51: 589-591 https://doi.org/10.1007/BF02128749
  2. Cha, S. H., A. Fukushima, K. Sakuma, and Y. Kagawa. 2001. Chronic docosahexaenoic acid intake enhances expression of the gene for uncoupling protein 3 and affects pleiotropic mRNA levels in skeletal muscle in aged C57BL/6NJcl mice. J. Nutr. 131: 2636-2642
  3. Cheung, P. C. K. 1996. The hypocholesterolemic effect of extracellular polysaccharide from the submerged fermentation ofmushroom. Nutr. Res. 16: 1953-1957 https://doi.org/10.1016/S0271-5317(96)00218-7
  4. Clapham, J. C., J. R. Arch, H. Chapman, A. Haynes, C. Lister, G B. Moore, V. Piercy, S. A. Carter, I. Lehner, and S. A. Smith. 2000. Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature 406: 415-418 https://doi.org/10.1038/35019082
  5. Dijkgraaf, G J. P., H. Li, and H. Bussey. 2002. Cell-wall ${\beta}$-glucan of Saccharomyces cerevisiae, pp. 179-205. In Erick Vandamme, Sophie De Baets, and Alexander Steinbuchel (eds.), Biopolymers, Vol. 6. Wiley-VCH Verlag Gmbh, Germany
  6. Foodand Drug Administration. 1996. Food labeling: Health claims: Oats and coronary heart disease. Fed. Regist. 61: 296-313
  7. Gong, D. W., S. Monemdjou, O. Gavrilova, J. R. Leon, B. Marcus-Samuels, C. J. Chou, C. Everett, J. P. Kozak, C. Li, and C. Deng. 2000. Lack of obesity and normal response to fasting and thyroid hormone in mice lacking uncoupling protein-3.1. Biol. Chem. 275: 16251-16257 https://doi.org/10.1074/jbc.M910177199
  8. Hong, K. H., S. A. Kang, S. H. Kim, and R. W. Choue. 2001 Effects of high fat diet on serum leptin and insulin level and brown adipose tissue UCP 1 expression in rats. Korean J. Nutrition 34: 865-871
  9. Jang, K. H., S. A. Kang, Y. Cho, Y. Y. Kim, Y. J. Lee, K.. Hong, K. W. Seong, S. H. Kim, C. H. Kim, S. K. Rhee, S. D. Ha, and R. W. Choue. 2003. Prebiotics properties oflevan in rats. J. Microbiol. Biotechnol. 13: 348-353
  10. Kang, S. A., J. C. Lee, Y. M. Park, C. Lee, S.-H. Kim, B.-I. Chang, C. H. Kim, J.-w. Seo, S.-K. Rhee, S. J. Jung, S.-M. Kim, S. K. Park, and K.-H. Jang. Secretory production of Rahnella aquatilis ATCC 33071 levansucrase expressed in Escherichia coli. J. Microbiol. Biotechnol. 14: 1232-1238
  11. Kang, S. A., K. Hong, K. H. Jang, S. H. Kim, K. H. Lee, B. I. Chang, C. H. Kim, and R. Choue. 2004. Anti-obesity and hypolipidemic effects of dietary levan in high fat diet-induced obese rats. J. Microbiol. Biotechnol. 14: 796-804
  12. Kim, H. N., J. N. Lee, G E. Kim, Y. M. Ha-Lee, C. W. Kim, and J. Sohn. 1999. Comparative study of the immune-enhancing activity of crude and mannoprotein-free yeast-glucan preparations. J. Microbiol. Biotechnol. 9: 826-831
  13. Kim, M. K., K. E. Ryu, W. A. Choi, Y. H. Rhee, and I. Y. Lee. 2003. Enhanced production of (13)-${\beta}$-D-glucan by a mutant strain of Agrobacterium species. Biochem. Eng. J. 3730: 1-6
  14. Klein S, J. F. Horowitz, M. Landt, S. J. Goodrick, V. Mohamed-AJi, and S. W. Coppack. 2000. Leptin production during early starvation in lean and obese women. Am. J. Physiol. Endocrinol. Metab. 278: E280-284 https://doi.org/10.1152/ajpendo.2000.278.2.E280
  15. Lairon, D. 1996. Dietary fibres: Effects on lipid metabolism and mechanisms of action. Eur. J. Clin. Nutr. 50: 125-133
  16. Lavau, M., C. Susin, J. Knittle, H. S. Blanchet, and M. R. C. Greenwood. 1977. A reliable photomicrographic method for determining fat cell size and number: Application to dietary obesity. Proc. Soc. Exp. Biol. Med. 156: 251-256
  17. Lee, I. Y. 2002. Curdlan, pp. 135-158. In Erick Vandamme, Sophie De Baets, and Alexander Steinbuchel (eds.), Biopolymers, Vol. 5. Wiley-VCH Verlag Gmbh, Germany
  18. Li, B., L. A. Nolte, J. S. Ju, D. H. Han, T. Coleman, J. O. Holloszy, and C. F. Semenkovich. 2000. Skeletal muscle respiratory uncoupling prevents diet-induced obesity and insulin resistance in mice. Nature Med. 6: 1115-1120 https://doi.org/10.1038/80450
  19. Llado, I., A. Pons, and A. Palou. 1997. Fatty acid composition of brown adipose tissue in dietary obese rats. Biochem. Mol. Biol. Int. 43: 1129-1136
  20. Lovegrove, J. A., A. Clohessy, H. Milon, and C. M. Williams. 2000. Modest doses of ${\beta}$-glucan do not reduce concentrations of potentially atherogenic lipoproteins. Am. J. Clin. Nutr. 72: 49-55 https://doi.org/10.1093/ajcn/72.1.49
  21. Mistry, A. M., A. G Swcik, and D. R. Romsos. 1997. Leptin rapidly lowers food intake and elevates metabolic rates in lean and oblbo mice. J. Nutr. 127: 2065-2072
  22. Nicolosi, R., S. J. Bell, B. R. Bistrian, J. Greenberg, R. A. Forse, and G L. Blackburn. 1999. Plasma lipid changes after supplementation with ${\beta}$-glucan fiber from yeast. Am. J. Clin. Nutr. 70: 208-212 https://doi.org/10.1093/ajcn.70.2.208
  23. Rippe, C., K. Berger, C. Boeirs, D. Ricquier, and A. C. Erlanson. 2000. Effect of high-fat diet, surrouding temperature, and enterostatin on uncoupling protein gene expression. Am. J. Physiol. Endocrinol. Metab. 279: E293-E300 https://doi.org/10.1152/ajpendo.2000.279.2.E293
  24. Seog, H. M., S. R. Kim, H. D. Choi, and H. M. Kim. 2002. Effects of ${\beta}$-glucan-enriched barley fraction on the lipid and cholesterol contents of plasma and feces in rat. Korean J. Food Sci. Technol. 34: 678-683
  25. Shimizu, J., N. Tsuchihashi, K. Kudoh, M. Wada, T. Tajita, and S. Innami. 2001. Dietary curdlan increases proliferation of Bijidobacteria cecum of rats. Biosci. Biotechnol. Biochem. 65: 466-469 https://doi.org/10.1271/bbb.65.466
  26. Wolever, T., P. Spadafora, S. Cunnane, and P. Pencharz. 1995. Propionate inhibits incorporation of colonic [1,2-$^{13}C$]acetate into plasma lipids in humans. Am. J. Clin. Nutr. 61: 1241-1247 https://doi.org/10.1093/ajcn/61.6.1241
  27. Wright, R. S., J. W. Anderson, and S. R. Briges. 1990. Propionate inhibit hepatocyte lipid synthesis. Proc. Soc. Exp. Biol. Med. 195: 26-29
  28. Yang, B. K., S. C. Jeong, and C. H. Song. 2002. Hypolipidemic effects of exo- and endo-biopolymers produced from submerged mycelial culture of Ganoderma lucidum in rats. J. Microbiol. Biotechnol. 12: 872-877
  29. Yang, B. K., J. B. Park, and C. H. Song. 2002. Hypolipidemic effect of exo-polymer produced in submerged mycelial culture of five different mushrooms. J. Microbiol. Biotechnol. 12: 957-961