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Evidence-Based Complementary and Alternative Medicine
Volume 2014, Article ID 705636, 15 pages
http://dx.doi.org/10.1155/2014/705636
Research Article

Validation of the Antidiabetic and Hypolipidemic Effects of Clitocybe nuda by Assessment of Glucose Transporter 4 and Gluconeogenesis and AMPK Phosphorylation in Streptozotocin-Induced Mice

1Graduate Institute of Pharmaceutical Science and Technology, College of Health Science, Central Taiwan University of Science and Technology, No. 666 Buzih Road, Beitun District, Taichung City 40601, Taiwan
2Plant Pathology Division, Taiwan Agricultural Research Institute, Council of Agriculture, Executive Yuan, Wufeng District, Taichung City 41362, Taiwan
3Department of Internal Medicine, Fengyuan Hospital, Ministry of Health and Welfare, Fengyuan District, Taichung City 42055, Taiwan

Received 11 November 2013; Accepted 4 December 2013; Published 3 February 2014

Academic Editor: Ha Won Kim

Copyright © 2014 Chun-Ching Shih et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. Barros, B. A. Venturini, P. Baptista, L. M. Estevinho, and I. C. F. R. Ferreira, “Chemical composition and biological properties of Portuguese wild mushrooms: a comprehensive study,” Journal of Agricultural and Food Chemistry, vol. 56, no. 10, pp. 3856–3862, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. B. Dulger, C. C. Ergul, and F. Gucin, “Antimicrobial activity of the macrofungus Lepista nuda,” Fitoterapia, vol. 73, no. 7-8, pp. 695–697, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. M. A. Murcia, M. Martínez-Tomé, A. M. Jiménez, A. M. Vera, M. Honrubia, and P. Parras, “Antioxidant activity of edible fungi (truffles and mushrooms): losses during industrial processing,” Journal of Food Protection, vol. 65, no. 10, pp. 1614–1622, 2002. View at Google Scholar · View at Scopus
  4. J. T. Chen, H. J. Su, and J. W. Huang, “Isolation and identification of secondary metabolites of Clitocybe nuda inhibition of zoospore germination of Phytophthora capsici,” Journal of Agricultural and Food Chemistry, vol. 60, no. 30, pp. 7341–7344, 2012. View at Publisher · View at Google Scholar
  5. D. Xu, Y. Sheng, Z.-Y. Zhou, R. Liu, Y. Leng, and J.-K. Liu, “Sesquiterpenes from cultures of the basidiomycete Clitocybe conglobata and their 11β-hydroxysteroid dehydrogenase inhibitory activity,” Chemical and Pharmaceutical Bulletin, vol. 57, no. 4, pp. 433–435, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. D. J. St. Jean Jr., M. Wang, and C. Fotsch, “Inhibitors of 11β-HSD1: a potential treatment for the metabolic syndrome,” Current Topics in Medicinal Chemistry, vol. 8, no. 17, pp. 1508–1523, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Wild, G. Roglic, A. Green, R. Sicree, and H. King, “Global prevalence of diabetes: estimates for the year 2000 and projections for 2030,” Diabetes Care, vol. 27, no. 5, pp. 1047–1053, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. K. C. Tomlinson, S. M. Gardiner, R. A. Hebden, and T. Bennett, “Functional consequences of streptozotocin-induced diabetes mellitus, with particular reference to the cardiovascular system,” Pharmacological Reviews, vol. 44, no. 1, pp. 103–150, 1992. View at Google Scholar · View at Scopus
  9. H. Yin, J. Miao, and Y. Zhang, “Protective effect of β-casomorphin-7 on type 1 diabetes rats induced with streptozotocin,” Peptides, vol. 31, no. 9, pp. 1725–1729, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Elsner, B. Guldbakke, M. Tiedge, R. Munday, and S. Lenzen, “Relative importance of transport and alkylation for pancreatic beta-cell toxicity of streptozotocin,” Diabetologia, vol. 43, no. 12, pp. 1528–1533, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Szkudelski, “The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas,” Physiological Research, vol. 50, no. 6, pp. 537–546, 2001. View at Google Scholar · View at Scopus
  12. M. Mueckler, “Facilitative glucose transporters,” European Journal of Biochemistry, vol. 219, no. 3, pp. 713–725, 1994. View at Google Scholar · View at Scopus
  13. N. J. Bryant, R. Govers, and D. E. James, “Regulated transport of the glucose transporter GLUT4,” Nature Reviews, vol. 3, no. 4, pp. 267–277, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. W. Lee, J. Ryu, R. P. Souto, P. F. Pilch, and C. Y. Jung, “Separation and partial characterization of three distinct intracellular GLUT4 compartments in rat adipocytes. Subcellular fractionation without homogenization,” The Journal of Biological Chemistry, vol. 274, no. 53, pp. 37755–37762, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. R. T. Watson and J. E. Pessin, “Intracellular organization of insulin signaling and GLUT4 translocation,” Recent Progress in Hormone Research, vol. 56, pp. 175–193, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Sujatha, S. Anand, K. N. Sangeetha et al., “Biological evaluation of (3β)-stigmast-5-en-3-ol as potent anti-diabetic agent in regulating glucose transport using in vitro model,” International Journal of Diabetes Mellitus, vol. 2, no. 2, pp. 101–109, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Huang and M. P. Czech, “The GLUT4 glucose transporter,” Cell Metabolism, vol. 5, no. 4, pp. 237–252, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Foretz, N. Toleux, B. Guigas et al., “Regulation of energy metabolism by AMPK: a novel therapeutic approach for the treatment of metabolic and cardiovascular diseases,” Médecine Sciences, vol. 22, no. 4, pp. 381–388, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. B. Viollet, L. Lantier, J. Devin-Leclerc et al., “Targeting the AMPK pathway for the treatment of type 2 diabetes,” Frontiers in Bioscience, vol. 14, no. 9, pp. 3380–3400, 2009. View at Google Scholar · View at Scopus
  20. G. Zhou, R. Myers, Y. Li et al., “Role of AMP-activated protein kinase in mechanism of metformin action,” The Journal of Clinical Investigation, vol. 108, no. 8, pp. 1167–1174, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. S. C. Stein, A. Woods, N. A. Jones, M. D. Davison, and D. Cabling, “The regulation of AMP-activated protein kinase by phosphorylation,” Biochemical Journal, vol. 345, no. 3, pp. 437–443, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Swain and W. E. Hills, “The phenolic constituents of Punnus domestica. I. Quantitative analysis of phenolic constituents,” Journal of the Science of Food and Agriculture, vol. 10, no. 1, pp. 63–68, 1959. View at Publisher · View at Google Scholar
  23. M. Dubois, K. A. Gilles, J. K. Hamilton, P. A. Rebers, and F. Smith, “Colorimetric method for determination of sugars and related substances,” Analytical Chemistry, vol. 28, no. 3, pp. 350–356, 1956. View at Publisher · View at Google Scholar · View at Scopus
  24. Q. W. Shen, C. S. Jones, N. Kalchayanand, M. J. Zhu, and M. Du, “Effect of dietary α-lipoic acid on growth, body composition, muscle pH, and AMP-activated protein kinase phosphorylation in mice,” Journal of Animal Science, vol. 83, no. 11, pp. 2611–2617, 2005. View at Google Scholar · View at Scopus
  25. K. J. Raser, A. Posner, and K. K. W. Wang, “Casein zymography: a method to study μ-calpain, m-calpain, and their inhibitory agents,” Archives of Biochemistry and Biophysics, vol. 319, no. 1, pp. 211–216, 1995. View at Publisher · View at Google Scholar · View at Scopus
  26. U. K. Laemmli, “Cleavage of structural proteins during the assembly of the head of bacteriophage T4,” Nature, vol. 227, no. 5259, pp. 680–685, 1970. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Hayashi, R. Kojima, and M. Ito, “Strain differences in the diabetogenic activity of streptozotocin in mice,” Biological and Pharmaceutical Bulletin, vol. 29, no. 6, pp. 1110–1119, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. N. F. Wiernsperger, “Preclinical pharmacology of biguanides,” in Oral Antidiabetics, J. Kuhlmann and W. Pulus, Eds., vol. 119, chapter 12, pp. 305–358, Springer, Berlin, Germany, 1996. View at Publisher · View at Google Scholar
  29. S.-H. Liu, Y.-H. Chang, and M.-T. Chiang, “Chitosan reduces gluconeogenesis and increases glucose uptake in skeletal muscle in streptozotocin-induced diabetic rats,” Journal of Agricultural and Food Chemistry, vol. 58, no. 9, pp. 5795–5800, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. J. S. Choi, T. Yokozawa, and H. Oura, “Improvement of hyperglycemia and hyperlipemia in streptozotocin-diabetic rats by a methanolic extract of Prunus davidiana stems and its main component, prunin,” Planta Medica, vol. 57, no. 3, pp. 208–211, 1991. View at Google Scholar · View at Scopus
  31. S. R. Sharma, S. K. Dwivedi, and D. Swarup, “Hypoglycaemic and hypolipidemic effects of Cinnamomum tamala Nees leaves,” Indian Journal of Experimental Biology, vol. 34, no. 4, pp. 372–374, 1996. View at Google Scholar · View at Scopus
  32. D. E. Goldstein, R. R. Little, R. A. Lorenz, J. I. Malone, D. Nathan, and C. M. Peterson, “Tests of glycemia in diabetes,” Diabetes Care, vol. 27, supplement 1, pp. S91–S93, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Howlett and M. Ashwell, “Glycemic response and health: summary of a workshop,” American Journal of Clinical Nutrition, vol. 87, no. 1, pp. 212S–216S, 2008. View at Google Scholar · View at Scopus
  34. A. G. Huebschmann, J. G. Regensteiner, H. Vlassara, and J. E. B. Reusch, “Diabetes and advanced glycoxidation end products,” Diabetes Care, vol. 29, no. 6, pp. 1420–1432, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. L. Al-Shamaony, S. M. Al-Khazraji, and H. A. A. Twaij, “Hypoglycaemic effect of Artemisia herba alba. II. Effect of a valuable extract on some blood parameters in diabetic animals,” Journal of Ethnopharmacology, vol. 43, no. 3, pp. 167–171, 1994. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Rajkumar, N. Srinivasan, K. Balasubramanian, and P. Govindarajulu, “Increased degradation of dermal collagen in diabetic rats,” Indian Journal of Experimental Biology, vol. 29, no. 11, pp. 1081–1083, 1991. View at Google Scholar · View at Scopus
  37. M. N. Chatterja and R. Shinde, Text Book of Medical Biochemisty, Jaypee Brothers Medical, New Delhi, India, 5th edition, 2002.
  38. R. R. Murray, D. K. Granner, O. A. Mayes, and V. W. Rodwell, Gluconeogenesis and the Control of Blood Glucose, Appleton and Lange, Stamford, Conn, USA, 2003.
  39. Y. Minokoshi, C. R. Kahn, and B. B. Kahn, “Tissue-specific ablation of the GLUT4 glucose transporter or the insulin receptor challenges assumptions about insulin action and hlucose homeostasis,” The Journal of Biological Chemistry, vol. 278, no. 36, pp. 33609–33612, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. H.-G. Joost, G. I. Bell, J. D. Best et al., “Nomenclature of the GLUT/SLC2A family of sugar/polyol transport facilitators,” American Journal of Physiology, vol. 282, no. 4, pp. E974–E976, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. P. Daisy, K. Balasubramanian, M. Rajalakshmi, J. Eliza, and J. Selvaraj, “Insulin mimetic impact of catechin isolated from Cassia fistula on the glucose oxidation and molecular mechanisms of glucose uptake on streptozotocin-induced diabetic Wistar rats,” Phytomedicine, vol. 17, no. 1, pp. 28–36, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. R. Kurukulasuriya, J. T. Link, D. J. Madar et al., “Prospects for pharmacologic inhibition of hepatic glucose production,” Current Medicinal Chemistry, vol. 10, no. 2, pp. 99–121, 2003. View at Google Scholar · View at Scopus
  43. J. M. Berg, J. L. Tymoczko, and L. Stryer, “Glycolysis and glyconeogenesis,” in Stryer Biochemistry, J. M. Berg and J. L. Tymoczko, Eds., pp. 425–464, W. H. Freeman, New York, NY, USA, 2001. View at Google Scholar
  44. L. Guignot and G. Mithieux, “Mechanisms by which insulin, associated or not with glucose, may inhibit hepatic glucose production in the rat,” American Journal of Physiology, vol. 277, no. 6, pp. E984–E989, 1999. View at Google Scholar · View at Scopus
  45. D. Thiebaud, E. Jacot, and R. A. DeFronzo, “The effect of graded doses of insulin on total glucose uptake, glucose oxidation, and glucose storage in man,” Diabetes, vol. 31, no. 11, pp. 957–963, 1982. View at Publisher · View at Google Scholar · View at Scopus
  46. P. Alberts, C. Nilsson, G. Selén et al., “Selective Inhibition of 11β-hydroxysteroid dehydrogenase type 1 improves hepatic insulin sensitivity in hyperglycemic mice strains,” Endocrinology, vol. 144, no. 11, pp. 4755–4762, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Giorgino, L. Laviola, and A. Leonardini, “Pathophysiology of type 2 diabetes: rationale for different oral antidiabetic treatment strategies,” Diabetes Research and Clinical Practice, vol. 68, supplement 1, pp. S22–S29, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. B. Staels and J.-C. Fruchart, “Therapeutic roles of peroxisome proliferator-activated receptor agonists,” Diabetes, vol. 54, no. 8, pp. 2460–2470, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Kato, N. Higuchi, and M. Enjoji, “Reduced hepatic expression of adipose tissue triglyceride lipase and CGI-58 may contribute to the development of non-alcoholic fatty liver disease in patients with insulin resistance,” Scandinavian Journal of Gastroenterology, vol. 43, no. 8, pp. 1018–1019, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Cases, S. J. Stone, P. Zhou et al., “Cloning of DGAT2, a second mammalian diacylglycerol acyltransferase, and related family members,” The Journal of Biological Chemistry, vol. 276, no. 42, pp. 38870–38876, 2001. View at Publisher · View at Google Scholar · View at Scopus
  51. Y. Minokoshi, Y.-B. Kim, O. D. Peroni et al., “Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase,” Nature, vol. 415, no. 6869, pp. 339–343, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. F. Bourgeois, A. Alexiu, and D. Lemonnier, “Dietary-induced obesity: effect of dietary fats on adipose tissue cellularity in mice,” British Journal of Nutrition, vol. 49, no. 1, pp. 17–26, 1983. View at Google Scholar · View at Scopus
  53. M.-Y. Wang, L. Chen, G. O. Clark et al., “Leptin therapy in insulin-deficient type I diabetes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 11, pp. 4813–4819, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. L. Woods, J. R. Petrie, and C. Sutherland, “Dissecting insulin signaling pathways: individualised therapeutic targets for diagnosis and treatment of insulin resistant states,” Endocrine, Metabolic & Immune Disorders, vol. 9, no. 2, pp. 187–198, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Suwa, T. Egashira, H. Nakano, H. Sasaki, and S. Kumagai, “Metformin increases the PGC-1α protein and oxidative enzyme activities possibly via AMPK phosphorylation in skeletal muscle in vivo,” Journal of Applied Physiology, vol. 101, no. 6, pp. 1685–1692, 2006. View at Publisher · View at Google Scholar · View at Scopus