Antidiabetic activity of Ganoderma lucidum polysaccharides F31 down-regulated hepatic glucose regulatory enzymes in diabetic mice

Journal of Ethnopharmacology

Volumn 196, Issue , 2017, Pages 47-57

  Xiao, Chun ^a   Wu, Qingping ^a   Zhang, Jumei ^a   Xie, Yizhen ^a   Cai, Wen ^b   Tan, Jianbin ^b  

^a GUANGDONG INSTITUTE OF MICROBIOLOGY   (China)

^b GUANGZHOU CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

Antidiabetic activity; Ganoderma lucidum polysaccharides; Hypoglycemic mechanism; Insulin resistance; Type 2 diabetes

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ANTIDIABETIC AGENT; FATTY ACID SYNTHASE; GANODERMA LUCIDUM POLYSACCHARIDE F21; GANODERMA LUCIDUM POLYSACCHARIDE F22; GANODERMA LUCIDUM POLYSACCHARIDE F31; GANODERMA LUCIDUM POLYSACCHARIDE F32; GLUCOSE; GLUCOSE TRANSPORTER 4; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; MESSENGER RNA; METFORMIN; POLYSACCHARIDE; RESISTIN; UNCLASSIFIED DRUG; ACC1 PROTEIN, MOUSE; FUNGAL POLYSACCHARIDE; GLUCOSE BLOOD LEVEL; SLC2A4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANTIDIABETIC ACTIVITY; ARTICLE; CONTROLLED STUDY; DIABETES CONTROL; DOWN REGULATION; EPIDIDYMIS FAT; GANODERMA LUCIDUM; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; INSULIN BLOOD LEVEL; MALE; MASS FRAGMENTOGRAPHY; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; POLYMERASE CHAIN REACTION; RANDOMIZED CONTROLLED TRIAL (TOPIC); WESTERN BLOTTING; ADIPOSE TISSUE; ANALYSIS; ANIMAL; BLOOD; C57BL MOUSE; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DIET RESTRICTION; DRUG EFFECTS; FRUITING BODY; GANODERMA; GENETICS; LIVER; METABOLISM;

ACETYL-COA CARBOXYLASE; ADIPOSE TISSUE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BLOOD GLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DOWN-REGULATION; FASTING; FATTY ACID SYNTHASE, TYPE I; FRUITING BODIES, FUNGAL; FUNGAL POLYSACCHARIDES; GANODERMA; GLUCOSE TRANSPORTER TYPE 4; HYPOGLYCEMIC AGENTS; INSULIN; LIVER; MALE; MICE, INBRED C57BL; RNA, MESSENGER;

EID: 85006726035     PISSN: 03788741     EISSN: 18727573     Source Type: Journal    
DOI: 10.1016/j.jep.2016.11.044     Document Type: Article

References (64)

1. Agius, L., New hepatic targets for glycaemic control in diabetes. Best. Pract. Res. Clin. Endocrinol. Metab. 21 (2007), 587–605.
2. Banerjee, R.R., Rangwala, S.M., Shapiro, J.S., Rich, A.S., Rhoades, B., Qi, Y., Wang, J., Rajala, M.W., Pocai, A., Scherer, P.E., Steppan, C.M., Ahima, R.S., Obici, S., Rossetti, L., Lazar, M.A., Regulation of fasted blood glucose by resistin. Science 303 (2004), 1195–1198.
3. Brink, M., Price, S.R., Chrast, J., Bailey, J.L., Anwar, A., Mitch, W.E., Delafontaine, P., Angiotensin II induces skeletal muscle wasting through enhanced protein degradation and down-regulates autocrine insulin-like growth factor I. Endocrinology 142 (2001), 1489–1496.
4. Boh, B., Berovic, M., Zhang, J., Zhi-Bin, L., Ganoderma lucidum and its pharmaceutically active compounds. Biotechnol. Annu. Rev. 13 (2007), 265–301.
5. Chema, B., Fabienne, F., Guilhem, J., Jacqueline, D., Luc, W., Michel, P., Christophe, B., Philippe, T., Structural Characterization, Technological Functionality and Physiological Aspects of Fungal beta-D-Glucans: A Review. Crit. Rev. Food Sci. Nutr. 56, 2016,1746–1752.
6. Chen, J., Raymond, K., Beta-glucans in the treatment of diabetes and associated cardiovascular risks. Vasc. Health Risk Manag 4 (2008), 1265–1272.
7. Chen, J., Seviour, R., Medicinal importance of fungal beta-(1->3), (1->6)-glucans. Mycol. Res. 111 (2007), 635–652.
8. Chen, L., Jiao, Z.H., Zheng, L.S., Zhang, Y.Y., Xie, S.T., Wang, Z.X., Wu, J.W., Structural insight into the autoinhibition mechanism of AMP-activated protein kinase. Nature, 459, 2009 (1146-U1139).
9. Cugnet-Anceau, C., Nazare, J.A., Biorklund, M., Le Coquil, E., Sassolas, A., Sothier, M., Holm, J., Landin-Olsson, M., Onning, G., Laville, M., Moulin, P., A controlled study of consumption of beta-glucan-enriched soups for 2 months by type 2 diabetic free-living subjects. Br. J. Nutr. 103 (2010), 422–428.
10. De Silva, D.D., Rapior, S., Hyde, K.D., Bahkali, A.H., Medicinal mushrooms in prevention and control of diabetes mellitus. Fungal Divers 56 (2012), 1–29.
11. Djaouti, L., Jourdan, T., Demizieux, L., Chevrot, M., Gresti, J., Verges, B., Degrace, P., Different effects of pioglitazone and rosiglitazone on lipid metabolism in mouse cultured liver explants. Diabetes Metab. Res. Rev. 26 (2010), 297–305.
12. Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F., Colorimetric method for determination of sugars and related substances. Anal. Chem. 28 (1956), 350–356.
13. Fruhbeck, G., Gomez-Ambrosi, J., Muruzabal, F.J., Burrell, M.A., The adipocyte: a model for integration of endocrine and metabolic signaling in energy metabolism regulation. Am. J. Physiol. Endocrinol. Metab. 280 (2001), E827–E847.
14. Hatanaka, K., Song, S.C., Maruyama, A., Kobayashi, A., Kuzuhara, H., Akaike, T., A New Synthetic Hypoglycemic Polysaccharide. Biochem. Biophys. Res. Commun. 188 (1992), 16–19.
15. Hawley, S.A., Davison, M., Woods, A., Davies, S.P., Beri, R.K., Carling, D., Hardie, D.G., Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J. Biol. Chem. 271 (1996), 27879–27887.
16. Hegarty, B.D., Furler, S.M., Ye, J., Cooney, G.J., Kraegen, E.W., The role of intramuscular lipid in insulin resistance. Acta Physiol. Scand. 178 (2003), 373–383.
17. Hikino, H., Ishiyama, M., Suzuki, Y., Konno, C., Antidiabetic drugs 0.33. mechanisms of hypoglycemic activity of ganoderan-B - a glycan of ganoderma-lucidum fruit bodies. Planta Med., 1989, 423–428.
18. Hikino, H., Konno, C., Mirin, Y., Hayashi, T., Antidiabetes drugs 0.9. isolation and hypoglycemic activity of ganoderans-a and ganoderans-B, glycans of ganoderma-lucidum fruit bodies. Planta Med., 1985, 339–340.
19. Huang, X.L., Wu, H.Q., Huang, F., Lin, X.S., Analysis of polysaccharide from broken cellular wall and unbroken spore of Ganoderma lucidum. Chin. Tradit. Herb. Drugs 37 (2006), 813–816.
20. Kang, S.I., Jin, Y.J., Ko, H.C., Choi, S.Y., Hwang, J.H., Whang, I., Kim, M.H., Shin, H.S., Jeong, H.B., Kim, S.J., Petalonia improves glucose homeostasis in streptozotocin-induced diabetic mice. Biochem. Biophys. Res. Commun. 373 (2008), 265–269.
21. Kennaway, D.J., Owens, J.A., Voultsios, A., Boden, M.J., Varcoe, T.J., Metabolic homeostasis in mice with disrupted Clock gene expression in peripheral tissues. Am. J. Physiol.-Reg. I 293 (2007), R1528–R1537.
22. Kiho, T., Kobayashi, T., Morimoto, H., Usui, S., Ukai, S., Hirano, K., Aizawa, K., Inakuma, T., Structural features of an anti-diabetic polysaccharide (TAP) from Tremella aurantia. Chem. Pharm. Bull. 48 (2000), 1793–1795.
23. Kiho, T., Morimoto, H., Kobayashi, T., Usui, S., Ukai, S., Aizawa, K., Inakuma, T., Effect of a polysaccharide (TAP) from the fruiting bodies of Tremella aurantia on glucose metabolism in mouse liver. Biosci. Biotechnol. Biochem. 64 (2000), 417–419.
24. Kiho, T., Morimoto, H., Sakushima, M., Usui, S., Ukai, S., Polysaccharides in fungi 0.35. Anti diabetic activity of an acidic polysaccharide from the fruiting bodies of Tremella aurantia. Biol. Pharm. Bull. 18 (1995), 1627–1629.
25. Kiho, T., Watanabe, T., Nagai, K., Ukai, S., Hypoglycemic activity of polysaccharide fraction from rhizome of rehmannia-glutinosa libosch F-hueichingensis hsiao and the effect on carbohydrate-metabolism in normal mouse-liver. Yakugaku Zasshi-J. Pharm. Soc. Jpn. 112 (1992), 393–400.
26. Kim, K.M., Lee, K.S., Lee, G.Y., Jin, H., Durrance, E.S., Park, H.S., Choi, S.H., Park, K.S., Kim, Y.B., Jang, H.C., Lim, S., Anti-diabetic efficacy of KICG1338, a novel glycogen synthase kinase-3beta inhibitor, and its molecular characterization in animal models of type 2 diabetes and insulin resistance. Mol. Cell Endocrinol. 409 (2015), 1–10.
27. Kim, Y.W., Kim, K.H., Choi, H.J., Lee, D.S., Anti-diabetic activity of beta-glucans and their enzymatically hydrolyzed oligosaccharides from Agaricus blazei. Biotechnol. Lett. 27 (2005), 483–487.
28. Laroche, C., Michaud, P., New developments and prospective applications for beta (1,3) glucans. Recent Pat. Biotechnol. 1 (2007), 59–73.
29. Lei, H., Ma, X., Wu, W.T., Anti-diabetic effect of an alpha-glucan from fruit body of maitake (Grifola frondosa) on KK-Ay mice. J. Pharm. Pharm. 59 (2007), 575–582.
30. Li, J.B., Wassner, S.J., Protein-synthesis and degradation in skeletal-muscle of chronically uremic rats. Kidney Int. 29 (1986), 1136–1143.
31. Li, W.L., Zheng, H.C., Bukuru, J., De Kimpe, N., Natural medicines used in the traditional Chinese medical system for therapy of diabetes mellitus. J. Ethnopharmacol. 92 (2004), 1–21.
32. −ΔΔCT method. Methods 25 (2001), 402–408.
33. Lo, H.C., Wasser, S.P., Medicinal mushrooms for glycemic control in diabetes mellitus: history,history, current status, future perspectives, and unsolved problems (Review). Int. J. Med. Mushrooms 13 (2011), 401–426.
34. Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., Protein measurement with the folin phenol reagent. J. Biol. Chem. 193 (1951), 265–275.
35. Ma, H.T., Hsieh, J.F., Chen, S.T., Anti-diabetic effects of Ganoderma lucidum. Phytochemistry 114 (2015), 109–113.
36. Manohar, V., Talpur, N.A., Echard, B.W., Lieberman, S., Preuss, H.G., Effects of a water-soluble extract of maitake mushroom on circulating glucose/insulin concentrations in KK mice. Diabetes Obes. Metab. 4 (2002), 43–48.
37. Moore, G.B.T., Chapman, H., Holder, J.C., Lister, C.A., Piercy, V., Smith, S.A., Clapham, J.C., Differential regulation of adipocytokine mRNAs by rosiglitazone in db/db mice. Biochem. Biophys. Res. Commun. 286 (2001), 735–741.
38. Morinaga, H., Yamamoto, H., Sakata, K., Fukuda, S., Ito, M., Sasase, T., Miyajima, K., Ueda, N., Ohta, T., Matsushita, M., Characterization of hepatic glucose metabolism disorder with the progress of diabetes in male spontaneously diabetic torii rats. J. Vet. Med. Sci. 70 (2008), 1239–1245.
39. Oclon, E., Zubel-Lojek, J., Latacz, A., Pierzchala-Koziec, K., Hyperglycemia-induced changes in resistin gene expression in white adipose tissue in piglets. Ann. Anim. Sci. 15 (2015), 667–679.
40. Pan, D., Zhang, D., Wu, J.S., Chen, C.H., Xu, Z.X., Yang, H.J., Zhou, P., Antidiabetic, antihyperlipidemic and antioxidant activities of a novel proteoglycan from ganoderma lucidum fruiting bodies on db/db mice and the possible mechanism. PLoS One, 8, 2013.
41. Ronnebaum, S.M., Joseph, J.W., Ilkayeva, O., Burgess, S.C., Lu, D., Becker, T.C., Sherry, A.D., Newgard, C.B., Chronic suppression of acetyl-CoA carboxylase 1 in beta-cells impairs insulin secretion via inhibition of glucose rather than lipid metabolism. J. Biol. Chem. 283 (2008), 14248–14256.
42. Ros, J.L., Francini, F., Schinella, G.R., Natural products for the treatment of type 2 diabetes mellitus. Planta Med. 81 (2015), 975–994.
43. Samuel, V.T., Choi, C.S., Phillips, T.G., Romanelli, A.J., Geisler, J.G., Bhanot, S., McKay, R., Monia, B., Shutter, J.R., Lindberg, R.A., Shulman, G.I., Veniant, M.M., Targeting Foxo1 in mice using antisense oligonucleotide improves hepatic and peripheral insulin action. Diabetes 55 (2006), 2042–2050.
44. Sanz, P., AMP-activated protein kinase: structure and regulation. Curr. Protein Pept. Sci. 9 (2008), 478–492.
45. Seto, S.W., Lam, T.Y., Tam, H.L., Au, A.L.S., Chan, S.W., Wu, J.H., Yu, P.H.F., Leung, G.P.H., Ngai, S.M., Yeung, J.H.K., Leung, P.S., Lee, S.M.Y., Kwan, Y.W., Novel hypoglycemic effects of Ganoderma lucidum water-extract in obese/diabetic (+db/+db) mice. Phytomedicine (Jena.) 16 (2009), 426–436.
46. Srinivasan, K., Viswanad, B., Asrat, L., Kaul, C.L., Ramarao, P., Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening. Pharm. Res. 52 (2005), 313–320.
47. Stein, S., Liehr, T., Eschrich, K., Characterization of the mouse liver fructose-1,6-bisphosphatase gene. Gene 264 (2001), 215–224.
48. Steppan, C.M., Bailey, S.T., Bhat, S., Brown, E.J., Banerjee, R.R., Wright, C.M., Patel, H.R., Ahima, R.S., Lazar, M.A., The hormone resistin links obesity to diabetes. Nature 409 (2001), 307–312.
49. Stevens, J.F., Determination of glucose by an automatic analyser. Clin. Chim. Acta 32 (1971), 199–201.
50. Teng, B.S., Wang, C.D., Yang, H.J., Wu, J.S., Zhang, D., Zheng, M., Fan, Z.H., Pan, D., Zhou, P., A Protein Tyrosine Phosphatase 1B Activity Inhibitor from the Fruiting Bodies of Ganoderma lucidum (Fr.) Karst and Its Hypoglycemic Potency on Streptozotocin-Induced Type 2 Diabetic Mice. J. Agric. Food Chem. 59 (2011), 6492–6500.
51. Teng, B.S., Wang, C.D., Zhang, D., Wu, J.S., Pan, D., Pan, L.F., Yang, H.J., Zhou, P., Hypoglycemic effect and mechanism of a proteoglycan from Ganoderma Lucidum on streptozotocin-induced type 2 diabetic rats. Eur. Rev. Med. Pharmacol. Sci. 16 (2012), 166–175.
52. Tomoda, M., Gonda, R., Kasahara, Y., Hikino, H., Antidiabetes drugs 0.23. glycan structures of ganoderan-B and ganoderan-C, hypoglycemic glycans of ganoderma-lucidum fruit bodies. Phytochemistry 25 (1986), 2817–2820.
53. Viollet, B., Andreelli, F., AMP-activated protein kinase and metabolic control. Handb. Exp. Pharm., 2011, 303–330.
54. Viollet, B., Lantier, L., Devin-Leclerc, J., Hebrard, S., Amouyal, C., Mounier, R., Foretz, M., Andreelli, F., Targeting the AMPK pathway for the treatment of Type 2 diabetes. Front. Biosci. (Landmark Ed.) 14 (2009), 3380–3400.
55. Wang, C.D., Teng, B.S., He, Y.M., Wu, J.S., Pan, D., Pan, L.F., Zhang, D., Fan, Z.H., Yang, H.J., Zhou, P., Effect of a novel proteoglycan PTP1B inhibitor from Ganoderma lucidum on the amelioration of hyperglycaemia and dyslipidaemia in db/db mice. Br. J. Nutr. 108 (2012), 2014–2025.
56. Wang, W.P., Guo, S.,Y., Li, L., Wang, M.L., Liang, G.,J., Determination of uronic acids in polysaccarides from Stanuntonia Chinensis. Food Sci. Technol. 10 (2007), 84–86.
57. Wu, C.M., Guo, Y.S., Su, Y., Zhang, X., Luan, H., Zhang, X.P., Zhu, H.X., He, H.X., Wang, X.L., Sun, G.B., Sun, X.B., Guo, P., Zhu, P., Cordycepin activates AMP-activated protein kinase (AMPK) via interaction with the gamma 1 subunit. J. Cell. Mol. Med. 18 (2014), 293–304.
58. Xiao, C., Wu, Q., Xie, Y., Zhang, J., Tan, J., Hypoglycemic effects of Grifola frondosa (Maitake) polysaccharides F2 and F3 through improvement of insulin resistance in diabetic rats. Food Funct. 6 (2015), 3567–3575.
59. Xiao, C., Wu, Q.P., Cai, W., Tan, J.B., Yang, X.B., Zhang, J.M., Hypoglycemic effects of Ganoderma lucidum polysaccharides in type 2 diabetic mice. Arch. Pharm. Res. 35 (2012), 1793–1801.
60. Ye, J.M., Iglesias, M.A., Watson, D.G., Ellis, B., Wood, L., Jensen, P.B., Sorensen, R.V., Larsen, P.J., Cooney, G.J., Wassermann, K., Kraegen, E.W., PPARalpha /gamma ragaglitazar eliminates fatty liver and enhances insulin action in fat-fed rats in the absence of hepatomegaly. Am. J. Physiol. Endocrinol. Metab. 284 (2003), E531–E540.
61. 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. Biotechnol. Biochem. 62 (1998), 1898–1903.
62. Zhang, B.B., Zhou, G.C., Li, C., AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab. 9 (2009), 407–416.
63. Zhao, M.M., Yang, N., Yang, B., Jiang, Y.M., Zhang, G.H., Structural characterization of water-soluble polysaccharides from Opuntia monacantha cladodes in relation to their anti-glycated activities. Food Chem. 105 (2007), 1480–1486.
64. Zheng, J.G., Gu, Y.J., Yan, S.P., Cai, D.C., Ma, L.G., Mu, D.H., Li, G.X., Pre-column derivatization and RP-HPLC determination of free amino acids in plasma and its application in inborn aminoacidopathies sreening. J. Instrum. Anal. 24 (2005), 22–25.