Hypoglycemic Effects of Fermented Chaga Mushroom (Inonotus obliquus) in the Diabetic Otsuka Long-Evans Tokushima Fatty (OLETF) Rat

  • Cha, Jae-Young (Alcoholic Beverage Research Institute, Daesun Distilling Co., Ltd.) ;
  • Jun, Bang-Sil (Department of Biotechnology, College of Natural Resources and Life Science, Dong-A University) ;
  • Kim, Jung-Wook (Department of Biotechnology, College of Natural Resources and Life Science, Dong-A University) ;
  • Park, Sang-Hyun (Department of Biotechnology, College of Natural Resources and Life Science, Dong-A University) ;
  • Lee, Chi-Hyeoung (Department of Biotechnology, College of Natural Resources and Life Science, Dong-A University) ;
  • Cho, Young-Su (Department of Biotechnology, College of Natural Resources and Life Science, Dong-A University)
  • Published : 2006.10.30

Abstract

Changes in the levels of analytes in the blood and urine of a rodent animal model were taken as a measure of the hypoglycemic effects of a diet containing fermented chaga mushroom. These studies were conducted using the genetically manipulated diabetic Otsuka Long-Evans Tokushima Fatty (OLETF) rat. The effects of 8-week long diets that included either fermented (FCM) or non-fermented (CM) chaga mushroom powder (5% in the diet) on the OLETF rat were compared to the normal diet fed OLETF rat and the non-diabetic Long-Evans Tokushima Otsuka (LETO) rat. Hypoglycemia was tracked by measuring serum and urine concentrations of glucose, insulin, fructosamine, and leptin. Serum and urine levels of glucose, fructosamine, and leptin in the OLETF rats were higher than in LETO rats when fed normal diets but insulin levels did not differ between the two animal groups. The FCM rats were characterized by dramatically low levels of serum glucose and leptin in the OLETF rats whereas the levels of fructosamine and urine glucose trended lower in response to FCM. The serum leptin level in the CM-fed OLETF rat was also lower than that in the normal diet fed OLETF control. Serum concentrations of insulin in the OLETF rats were higher following FCM or CM feeding compared to the normal diet. These observations imply that (a) a dietary supplement of fermented chaga mushroom may contribute to a hypoglycemic effect in the OLETF rat, and (b) the increased blood insulin concentration following 8 weeks of an FCM diet may be important to the noted improvement in hyperglycemia.

Keywords

References

  1. Chang ST. World production of cultivated edible and medicinal mushrooms in 1977 with emphasis on Lintinus edodes (Berk) Sig. in China. Int. J. Med. Mushroom 1: 291-300 (1999) https://doi.org/10.1615/IntJMedMushr.v1.i4.10
  2. Wong KH, Cheung PCK, Wu JZ. Biochemical and microstructural characteristics of insoluble and soluble dietary fiber prepared from mushroom sclerotia of Pleurotus tube-regium, Polyporus rhinoceros, and Wolfiporia cocos. J. Agr. Food Chem. 51: 7197-7202 (2003) https://doi.org/10.1021/jf034195g
  3. Wu YC, Hsu JH, Liu IM, Liou SS, Su HC, Cheng JT. Increase of insulin sensitivity in diabetic rats received Die-Huang-Wan, an herbal mixture used in Chinese traditional medicine. Acta Pharmacol. Sin. 23: 1181-1187 (2002)
  4. Manohar V, Talpur NA, Echard BW, Lieberman S, Preuss HG. Effects of a water-soluble extract of maitake mushroom on circulating glucose/insulin concentrations in KK mice. Diabetes Obes. Metab. 4: 43-48 (2002) https://doi.org/10.1046/j.1463-1326.2002.00180.x
  5. Yuan Z, He P, Cui J, Takeuchi H. Hypoglycemic effect of water-soluble polysaccharide from Auricularia auricula-judae Quel. on genetically diabetic KK-Ay mice. Biosci. Biotech. Bioch. 62: 1898-1903 (1998) https://doi.org/10.1271/bbb.62.1898
  6. Zhang HN, He JH, Yuan L, Lin ZB. In vitro and in vivo protective effects of Ganoderma lucidum polysaccharides on alloxan-induced pancreatic islets damage. Life Sci. 73: 2307-2319 (2003) https://doi.org/10.1016/S0024-3205(03)00594-0
  7. Taipur NA, Echard BW, Yasmin T, Bagchi D, Preuss HG. Effects of niacin-bound chromium, maitake mushroom fraction SX and (-)-hydroxycitric acid on the metabolic syndrome in aged diabetic Zucker fatty rats. Mol. Cell Biochem. 252: 369-377 (2003) https://doi.org/10.1023/A:1025564930088
  8. Kiho T, Morimoto H, Kobayashi T, Usui S, Ukai S, Aizawa K, Inakuma T. Effects of a polysaccharide (TPA) from the fruiting bodies of Tremella aurantia on glucose metabolism in mouse liver. Biosci. Biotech. Bioch. 64: 417-419 (2000) https://doi.org/10.1271/bbb.64.417
  9. Kiho T, Morimoto H, Sakushima M, Usui S, Ukai S. Polysaccharides in fungi XXXV. Antidiabetic activity of an acidic polysaccharide from the fruiting bodies of Tremella aurantia. Biol. Pharm. Bull 18: 1627-1629 (1995) https://doi.org/10.1248/bpb.18.1627
  10. Zhang HN, Lin ZB. Hypoglycemic effect of Ganoderma lucidum polysaccharides. Acta Pharmacol. Sin. 25: 191-195 (2004)
  11. Talpur NA, Echard BW, Fan AY, Jaffari O, Bagchi D, Preuss HG. Antihypertensive and metabolic effects of whole maitake mushroom powder and its fractions in two rat strains. Mol. Cell Biochem. 237: 129-136 (2002) https://doi.org/10.1023/A:1016503804742
  12. Na ML, Yap AT. Inhibition of human colon carcinoma development by lentinan from shiitake mushroom (Lentinus edodes). J. Altern. Comple. Med. 8: 581-589 (2002) https://doi.org/10.1089/107555302320825093
  13. Bobek P, Ozdin L, Kuniak L. Antioxidative effect of Oyster mushroom (Pleurotus ostreatus) in hypercholesterolemic rat. Pharmazie 50: 441-442 (1995)
  14. Mizuno T, Zhuang C, Abe K, Okamoto H, Kiho T, Ukai S, Leclerc S, Meijer L. Antitumor and hypoglycemic activities of polysaccharides from the Sclerotia and Mycelia of Inonotus obliquus (Pers.: Fe.) PIl. (Aphyllophoromycetideae). Int. J. Med. Mushroom 1: 301-316 (1999) https://doi.org/10.1615/IntJMedMushr.v1.i4.20
  15. Shivrina AN. Chemical characteristics of compounds extracted from Inonotus obliquus. Chem. Abstr. 66: 17271-17279 (1967)
  16. Cha JY, Jun BS, Yoo KS, Hahm JR, Cho YS. Fermented chaga mushroom (Inonotus obliquus) effects on hypolipidemia and hepatoprotection in Otsuka Long-Evans Tokushima Fatty (OLETF) rats. Food Sci. Biotechnol. 15: 122-127 (2006)
  17. Alles MA, de Roos NM, Bakz JC, van de Lisdonk E, Zock PL, Hautvast JGAL. Consumption of fructo-oligosaccharides dose not favorably affect blood glucose and serum lipid concentrations in patients with type 2 diabetes. Am. J. Clin. Nutr. 69: 64-69 (1999) https://doi.org/10.1093/ajcn/69.1.64
  18. Lu XJ, Chen XM, Fu DX, Cong W, Ouyang F. Effect of Amorphophallus konjac oligosaccharides on streptozotocin-induced diabetic model of isolated islets. Life Sci. 72: 711-719 (2002) https://doi.org/10.1016/S0024-3205(02)02303-2
  19. Lee HW, Park TS, Choi JW, Yi SY, Shin WS. Antidiabetic effects of chitosan oligosaccharides in neonatal STZ-induced noninsulin-dependent diabetes mellitus in rats. Biol. Pharm. Bull. 26: 1100-1103 (2003) https://doi.org/10.1248/bpb.26.1100
  20. Kim YW, Kim KH, Choi HJ, Lee DS. Anti-diabetic activity of beta-glucans and their enzymatically hydrolyzed oligosaccharides from medicinal mushroom Agaricus blazei. Biotechnol. Lett. 27: 483-487 (2005) https://doi.org/10.1007/s10529-005-2225-8
  21. Cha JY, Jeon BS, Park JW, Moon JC, Cho YS. Effect of fermented compositions containing Inonotus obliquus with Houttuynia cordata on growth of human AGS gastric and HCT-15 colon cancer cells. J. Korean Soc. Appl. Biol. Chem. 47: 202-207 (2004)
  22. Cha JY, Jun BS, Lee CH, Yu GS, Moon JC, Cho YS: Hypoglycemic and antioxidative effects of fermented chaga mushroom (Inonotus obliquus) on streptozotocin-induced diabetic rats. J. Life Sci. 15: 809-818 (2005) https://doi.org/10.5352/JLS.2005.15.5.809
  23. Kawano K, Hirashima T, Mori S, Saitoh Y, Kurosumi M, Natori T. Spontaneous long-term hyperglycemic rat with diabetic complications Otsuka Long-Evans Tokushima Fatty (OLETF) strain. Diabetes 41: 1422-1428 (1992) https://doi.org/10.2337/diabetes.41.11.1422
  24. Mizuno M, Morimoto K, Tsuchida H. Polysaccharides from Aguricus blazei stimulate lymphocyte T-cell subsets in mice. Biosci. Biotech. Bioch. 62: 434-437 (1998) https://doi.org/10.1271/bbb.62.434
  25. Duncan DB. Multiple range test for correlated and heteroscedastic means. Biometrics 13: 164-176 (1957) https://doi.org/10.2307/2527799
  26. Lee YT, Kim YS. Water-solubility of ${\beta}$-glucans in various edible mushrooms. J. Food Sci. Nutr. 10: 294-297 (2005) https://doi.org/10.3746/jfn.2005.10.3.294
  27. Kubok K, Aoki H, Naba N. Anti-diabetic activities present in the fruiting body of Grifola frondosa (mitake). Biol. Pharm. Bull. 17: 1106-1110 (1994) https://doi.org/10.1248/bpb.17.1106
  28. Bobek P, Ozdin L, Kajaba I. Dose-dependent hypocholesterolemic effect of oyster mushroom (Pleurotus ostreatus) in rats. Physiol. Res. 47: 327-329 (1997)
  29. Fukushima M, Ohashi T, Fujiwara Y, Sonoyama K, Nakano M. Cholesterol-lowering effects of maitake (Grofola frondosa) fiber, shiitake (Letinus edodes) fiber, and enokitake (Flammulina velutipes) fiber in rats. Exp. Biol. Med. 226: 758-765 (2001) https://doi.org/10.1177/153537020222600808
  30. Jeon BS, Park JW, Kim BK, Kim HK, Jung TS, Hahm JR, Kim DR, Cho YS, Cha JY. Fermented mushroom milk supplemented dietary fiber prevents the onset of obesity and hypertriglyceridemia in Otsuka Long-Evans Tokushima Fatty (OLETF) rats. Diabetes Obes. Metab. 7: 709-715 (2005) https://doi.org/10.1111/j.1463-1326.2005.00456.x
  31. Arao K, Wang YM, Inoue N, Hirata J, Cha JY, Nagao K, Yanagita T. Dietary effect of pomegranate seed oil rich in 9cis, 11trans, 13cis conjugated linolenic acid on lipid metabolism in obese, hyperlipidemic OLETF rats. Lipid Health Dis. 3: 24-31 (2004) https://doi.org/10.1186/1476-511X-3-24
  32. Jia DM, Tabaru A, Akiyama T, Ade S, Otsuki M. Fatty liver, chronic viral hepatities and autoimmune hepatities. Troglitazone prevents fatty changes of the liver in obese diabetic rats. J. Gastroen. Hepatol. 15: 1183-1191 (2000) https://doi.org/10.1046/j.1440-1746.2000.02316.x
  33. Hong EG, Noh HL, Lee SK, Chung YS, Lee KW, Kim HM. Insulin and glucose secretions and morphological change of pancreatic islets in OLETF rats, a model of type 2 diabetic mellitus. J. Korean Med. Sci. 17: 34-40 (2002)
  34. Chai YM, Rhee SJ. Effects of dietary oligosaccharide on the blood glucose and serum lipid composition in streptozotocin-induced diabetic rats. J. Korean Soc. Food Sci. Nutr. 30: 710-716 (2001)
  35. Johnson RN, Metcalf PA, Baker JR. Fructosamine. a new approach to the estimation of serum glycosylprotein. An index of diabetic control. Clini. Chimi. Acta 127: 87-95 (1982)
  36. Lo HC, Tsai FA, Wasser SP, Yang JG, Huang BM. Effects of ingested fruiting bodies, submerged culture biomass, and acidic polysaccharide glucuronoxylomannan of Tremella mesenterica Retz. : Fr. on glycemic responses in normal and diabetic rats. Life Sci. 78: 1957-1966 (2006) https://doi.org/10.1016/j.lfs.2005.08.033
  37. Rahman SM, Wang YM, Yotsumoto H, Cha JY, Han SY, Inoue S, Yanagita T. Effects of conjugated linoleic acid on serum leptin concentration, body-fat accumulation, and ${\beta}$-oxidation of fatty acid in OLETF rats. Nutrition 17: 385-390 (2001) https://doi.org/10.1016/S0899-9007(00)00584-0
  38. Halaas JL, Boozer C, Blair-West J, Fidahusein N, Denton DA, Friedman JM. Physiological response to long-term peripheral and central leptin infusion in lean and obese mice. P. Natl. Acad. Sci. USA 94: 8878-8883 (1997)
  39. Niimi M, Sato M, Yokote R, Tada S, Takahara J. Effects of central and peripheral injection of leptin on food intake and on brain fos expression in the Otsuka Long-Evans Tokushima Fatty rat with hyperleptinaemia. J. Neuroendocrinol. 11: 605-611 (1999) https://doi.org/10.1046/j.1365-2826.1999.00368.x
  40. Yang BK, Kim DH, Jeong SC, Das S, Choi YS, Shin JS, Lee SC, Song CH. Hypoglycemic effect of a Lentinus edodes exo-polymer produced from a submerged mycelial culture. Biosci. Biotech. Bioch. 66: 937-942 (2002) https://doi.org/10.1271/bbb.66.937
  41. Gray AM, Flatt PR. Insulin-releasing and insulin-like activity of Agaricus campestris (mushroom). J. Endocrinol. 157: 259-266 (1998) https://doi.org/10.1677/joe.0.1570259
  42. Hwang HJ, Kim SW, Lim JM, Joo JH, Kim HO, Kim HM, Yun JW. Hypoglycemic effect of crude exopolysaccharides produced by a medicinal mushroom Phellinus baumii in streptozotocin-induced diabetic rats. Life Sci. 76: 3069-3080 (2005) https://doi.org/10.1016/j.lfs.2004.12.019
  43. Hikino H, Ishiyama M, Suzuki Y, Konno C. Mechanisms of hypoglycemic activity of ganoderan B : a glycan of Ganodema lucidum fruit bodies. Planta Med. 55: 423-428 (1989) https://doi.org/10.1055/s-2006-962057
  44. Hu SH, Wang JC, Lien JL, Liaw ET, Lee MY. Antihyperglycemic effect of polysaccharide from fermented broth of Pleurotus citrinopileatus. App. Microbiol. Biot. 7: 1-7 (2005)
  45. Chen MD, Song YM, Lin PY. Zinc effects on hyperglycemia and hypoleptinemia in streptozotocin-induced diabetic mice. Horm. Metab. Res. 32: 107-109 (2000) https://doi.org/10.1055/s-2007-978600
  46. Chen MD, Liou SJ, Lin PY, Yang VC, Alexander PS, Lin WH. Effects of zinc supplementation on the plasma glucose level and insulin activity in genetically obese (ob/ob) mice. Biol. Trace Elem. Res. 61: 303-311 (1998) https://doi.org/10.1007/BF02789090