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Journal of Diabetes Research
Volume 2015, Article ID 723190, 10 pages
http://dx.doi.org/10.1155/2015/723190
Research Article

Hypoglycemic Activity through a Novel Combination of Fruiting Body and Mycelia of Cordyceps militaris in High-Fat Diet-Induced Type 2 Diabetes Mellitus Mice

1Graduate Institute of Medical Sciences, School of Medicine, Taipei Medical University, Taipei 110, Taiwan
2Stem Cell Research Center, Taipei Medical University, Taipei 110, Taiwan
3Graduate Institute of Biomedical Materials and Tissue Engineering, College of Oral Medicine, Taipei Medical University, Taipei 110, Taiwan
4Institute of Biotechnology, College of Engineering, Southern Taiwan University of Science and Technology, Yongkang District, Tainan, Taiwan
5Department of Microbiology and Immunology, School of Medicine, Taipei Medical University, Taipei 110, Taiwan

Received 5 May 2015; Revised 30 June 2015; Accepted 5 July 2015

Academic Editor: Bernard Portha

Copyright © 2015 Sung-Hsun Yu 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. E. Morales Villegas, “Syndrome X vs metabolic syndrome,” Archivos de Cardiología de México, vol. 76, supplement 4, pp. S173–S188, 2006. View at Google Scholar · View at Scopus
  2. K. L. Tucker and S. Buranapin, “Nutrition and aging in developing countries,” The Journal of Nutrition, vol. 131, no. 9, pp. 2417S–2423S, 2001. View at Google Scholar · View at Scopus
  3. T. Nakamura, T. Terajima, T. Ogata et al., “Establishment and pathophysiological characterization of type 2 diabetic mouse model produced by streptozotocin and nicotinamide,” Biological and Pharmaceutical Bulletin, vol. 29, no. 6, pp. 1167–1174, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Szkudelski, “Streptozotocin-nicotinamide-induced diabetes in the rat. Characteristics of the experimental model,” Experimental Biology and Medicine, vol. 237, no. 5, pp. 481–490, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Boquist, B. Hellman, A. Lernmark, and I. B. Taljedal, “Influence of the mutation ‘diabetes’ on insulin release and islet morphology in mice of different genetic backgrounds,” Journal of Cell Biology, vol. 62, no. 1, pp. 77–89, 1974. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Shafrir, “Development and consequences of insulin resistance: lessons from animals with hyperinsulinaemia,” Diabetes and Metabolism, vol. 22, no. 2, pp. 122–131, 1996. View at Google Scholar · View at Scopus
  7. V. R. Drel, N. Mashtalir, O. Ilnytska et al., “The leptin-deficient (ob/ob) mouse: a new animal model of peripheral neuropathy of type 2 diabetes and obesity,” Diabetes, vol. 55, no. 12, pp. 3335–3343, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. S. R. Commerford, M. E. Bizeau, H. McRae, A. Jampolis, J. S. Thresher, and M. J. Pagliassotti, “Hyperglycemia compensates for diet-induced insulin resistance in liver and skeletal muscle of rats,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 281, no. 5, pp. R1380–R1389, 2001. View at Google Scholar · View at Scopus
  9. X. Zhang, Y. Cui, L. Fang, and F. Li, “Chronic high-fat diets induce oxide injuries and fibrogenesis of pancreatic cells in rats,” Pancreas, vol. 37, no. 3, pp. e31–e38, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. P. I. Parekh, A. E. Petro, J. M. Tiller, M. N. Feinglos, and R. S. Surwit, “Reversal of diet-induced obesity and diabetes in C57BL/6J mice,” Metabolism: Clinical and Experimental, vol. 47, no. 9, pp. 1089–1096, 1998. View at Publisher · View at Google Scholar · View at Scopus
  11. U. Hoffler, K. Hobbie, R. Wilson et al., “Diet-induced obesity is associated with hyperleptinemia, hyperinsulinemia, hepatic steatosis, and glomerulopathy in C57Bl/6J mice,” Endocrine, vol. 36, no. 2, pp. 311–325, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. M. E. Shaul, G. Bennett, K. J. Strissel, A. S. Greenberg, and M. S. Obin, “Dynamic, M2-like remodeling phenotypes of CD11c+ adipose tissue macrophages during high-fat diet—induced obesity in mice,” Diabetes, vol. 59, no. 5, pp. 1171–1181, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. G. M. Reaven, “Why Syndrome X? From Harold Himsworth to the insulin resistance syndrome,” Cell Metabolism, vol. 1, no. 1, pp. 9–14, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. R. S. Sherwin, “Role of the liver in glucose homeostasis,” Diabetes Care, vol. 3, no. 2, pp. 261–265, 1980. View at Publisher · View at Google Scholar · View at Scopus
  15. R. A. DeFronzo, “Obesity is associated with impaired insulin-mediated potassium uptake,” Metabolism, vol. 37, no. 2, pp. 105–108, 1988. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Florez, J. Luo, S. Castillo-Florez et al., “Impact of metformin-induced gastrointestinal symptoms on quality of life and adherence in patients with type 2 diabetes,” Postgraduate Medicine, vol. 122, no. 2, pp. 112–120, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. D. S. H. Bell, H. R. Patil, and J. H. O'Keefe, “Divergent effects of various diabetes drugs on cardiovascular prognosis,” Reviews in Cardiovascular Medicine, vol. 14, no. 2–4, pp. e107–e122, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Kung and R. R. Henry, “Thiazolidinedione safety,” Expert Opinion on Drug Safety, vol. 11, no. 4, pp. 565–579, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Hollander, “Safety profile of acarbose, an alpha-glucosidase inhibitor,” Drugs, vol. 44, supplement 3, pp. 47–53, 1992. View at Google Scholar · View at Scopus
  20. Y. Bando, Y. Ushiogi, D. Toya, N. Tanaka, and M. Fujisawa, “Three diabetic cases of acute dizziness due to initial administration of voglibose,” Internal Medicine, vol. 37, no. 9, pp. 753–756, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. J. K. H. Cheung, J. Li, A. W. H. Cheung et al., “Cordysinocan, a polysaccharide isolated from cultured Cordyceps, activates immune responses in cultured T-lymphocytes and macrophages: signaling cascade and induction of cytokines,” Journal of Ethnopharmacology, vol. 124, no. 1, pp. 61–68, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Ohmori, K. Tamura, N. Ohgane et al., “The correlation between molecular weight and antitumor activity of galactosaminoglycan (CO-N) from Cordyceps ophioglossoides,” Chemical and Pharmaceutical Bulletin, vol. 37, no. 5, pp. 1337–1340, 1989. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Kiho, Y. Shiose, K. Nagai, and S. Ukai, “Polysaccharides in fungi. XXX. Antitumor and immunomodulating activities of two polysaccharides from the fruiting bodies of Armillariella tabescens,” Chemical and Pharmaceutical Bulletin, vol. 40, no. 8, pp. 2110–2114, 1992. View at Publisher · View at Google Scholar · View at Scopus
  24. J.-S. Zhu, G. M. Halpern, and K. Jones, “The scientific rediscovery of an ancient Chinese herbal medicine: cordyceps sinensis part I,” Journal of Alternative and Complementary Medicine, vol. 4, no. 3, pp. 289–303, 1998. View at Publisher · View at Google Scholar · View at Scopus
  25. J.-S. Zhu, G. M. Halpern, and K. Jones, “The scientific rediscovery of a precious ancient Chinese herbal regimen: cordyceps sinensis: part II,” Journal of Alternative and Complementary Medicine, vol. 4, no. 4, pp. 429–457, 1998. View at Publisher · View at Google Scholar · View at Scopus
  26. T. Kiho, K. Ookubo, S. Usui, S. Ukai, and K. Hirano, “Structural features and hypoglycemic activity of a polysaccharide (CS-F10) from the cultured mycelium of Cordyceps sinensis,” Biological and Pharmaceutical Bulletin, vol. 22, no. 9, pp. 966–970, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Kiho, A. Yamane, J. Hui, S. Usui, and S. Ukai, “Polysaccharides in fungi. XXXVI. Hypoglycemic activity of a polysaccharide (CS-F30) from the cultural mycelium of Cordyceps sinensis and its effect on glucose metabolism in mouse liver,” Biological and Pharmaceutical Bulletin, vol. 19, no. 2, pp. 294–296, 1996. View at Publisher · View at Google Scholar · View at Scopus
  28. W. C. Kan, H. Y. Wang, C. C. Chien et al., “Effects of extract from solid-state fermented Cordyceps sinensis on type 2 diabetes mellitus,” Evidence-Based Complementary and Alternative Medicine, vol. 2012, Article ID 743107, 10 pages, 2012. View at Publisher · View at Google Scholar
  29. I. Hong, P. Kang, K. Kim et al., “Fruit body formation on silkworm by Cordyceps militaris,” Mycobiology, vol. 38, no. 2, pp. 128–132, 2010. View at Publisher · View at Google Scholar
  30. H. Hur, “Chemical ingredients of cordyceps militaris,” Mycobiology, vol. 36, no. 4, pp. 233–235, 2008. View at Publisher · View at Google Scholar
  31. Y. Dong, T. Jing, Q. Meng et al., “Studies on the antidiabetic activities of cordyceps militaris extract in diet-streptozotocin-induced diabetic sprague-dawley rats,” BioMed Research International, vol. 2014, Article ID 160980, 11 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. H.-Y. Wang, W.-C. Kan, T.-J. Cheng, S.-H. Yu, L.-H. Chang, and J.-J. Chuu, “Differential anti-diabetic effects and mechanism of action of charantin-rich extract of Taiwanese Momordica charantia between type 1 and type 2 diabetic mice,” Food and Chemical Toxicology, vol. 69, pp. 347–356, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. J. R. Zierath and Y. Kawano, “The effect of hyperglycaemia on glucose disposal and insulin signal transduction in skeletal muscle,” Best Practice and Research: Clinical Endocrinology and Metabolism, vol. 17, no. 3, pp. 385–398, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. G. Dimitriadis, P. Mitron, V. Lambadiari, E. Maratou, and S. A. Raptis, “Insulin effects in muscle and adipose tissue,” Diabetes Research and Clinical Practice, vol. 93, supplement 1, pp. S52–S59, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Schoonjans, B. Staels, and J. Auwerx, “The peroxisome proliferator activated receptors (PPARs) and their effects on lipid metabolism and adipocyte differentiation,” Biochimica et Biophysica Acta—Lipids and Lipid Metabolism, vol. 1302, no. 2, pp. 93–109, 1996. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Sasase, M. G. Pezzolesi, N. Yokoi, T. Yamada, and K. Matsumoto, “Animal models of diabetes and metabolic disease,” Journal of Diabetes Research, vol. 2013, Article ID 281928, 2 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Y. Hui, B.-S. Wang, C. H. Shiow, and P.-D. Duh, “Comparison of protective effects between cultured Cordyceps militaris and natural Cordyceps sinensis against oxidative damage,” Journal of Agricultural and Food Chemistry, vol. 54, no. 8, pp. 3132–3138, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. G. Zhang, Y. Huang, Y. Bian, J. H. Wong, T. B. Ng, and H. Wang, “Hypoglycemic activity of the fungi Cordyceps militaris, Cordyceps sinensis, Tricholoma mongolicum, and Omphalia lapidescens in streptozotocin-induced diabetic rats,” Applied Microbiology and Biotechnology, vol. 72, no. 6, pp. 1152–1156, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. X. Liu, K. Huang, and J. Zhou, “Composition and antitumor activity of the mycelia and fruiting bodies of Cordyceps militaris,” Journal of Food and Nutrition Research, vol. 2, no. 2, pp. 74–79, 2014. View at Publisher · View at Google Scholar
  40. S.-J. Huang, S.-Y. Tsai, Y.-L. Lee, and J.-L. Mau, “Nonvolatile taste components of fruit bodies and mycelia of Cordyceps militaris,” LWT—Food Science and Technology, vol. 39, no. 6, pp. 577–583, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. I. P. Hong, P. D. Kang, K. Y. Kim et al., “Fruit body formation on silkworm by Cordyceps militaris,” Mycobiology, vol. 38, no. 2, pp. 128–132, 2010. View at Publisher · View at Google Scholar
  42. Y.-J. Ahn, S.-J. Park, S.-G. Lee, S.-C. Shin, and D.-H. Choi, “Cordycepin: selective growth inhibitor derived from liquid culture of Cordyceps militaris against Clostridium spp,” Journal of Agricultural and Food Chemistry, vol. 48, no. 7, pp. 2744–2748, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Nakamura, K. Shinozuka, and N. Yoshikawa, “Anticancer and antimetastatic effects of cordycepin, an active component of Cordyceps sinensis,” Journal of Pharmacological Sciences, vol. 127, no. 1, pp. 53–56, 2015. View at Publisher · View at Google Scholar
  44. M.-H. Jeong, C.-M. Lee, S.-W. Lee et al., “Cordycepin-enriched Cordyceps militaris induces immunomodulation and tumor growth delay in mouse-derived breast cancer,” Oncology Reports, vol. 30, no. 4, pp. 1996–2002, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. A. M. Sugar and R. P. McCaffrey, “Antifungal activity of 3′-deoxyadenosine (cordycepin),” Antimicrobial Agents and Chemotherapy, vol. 42, no. 6, pp. 1424–1427, 1998. View at Google Scholar · View at Scopus
  46. V. Y. Kryukov, O. N. Yaroslavtseva, I. M. Dubovskiy, M. V. Tyurin, N. A. Kryukova, and V. V. Glupov, “Insecticidal and immunosuppressive effect of ascomycete Cordyceps militaris on the larvae of the Colorado potato beetle Leptinotarsa decemlineata,” Biology Bulletin, vol. 41, no. 3, pp. 276–283, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Shin, S. Lee, J. Kwon et al., “Cordycepin suppresses expression of diabetes regulating genes by inhibition of lipopolysaccharide-induced inflammation in macrophages,” Immune Network, vol. 9, no. 3, pp. 98–105, 2009. View at Publisher · View at Google Scholar
  48. R. M. Berne, “The role of adenosine in the regulation of coronary blood flow,” Circulation Research, vol. 47, no. 6, pp. 807–813, 1980. View at Publisher · View at Google Scholar · View at Scopus
  49. P. Hollander, “Anti-diabetes and anti-obesity medications: effects on weight in people with diabetes,” Diabetes Spectrum, vol. 20, no. 3, pp. 159–165, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Poirier, T. D. Giles, G. A. Bray et al., “Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, no. 5, pp. 968–976, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. A. R. Saltiel and C. R. Kahn, “Insulin signalling and the regulation of glucose and lipid metabolism,” Nature, vol. 414, no. 6865, pp. 799–806, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. F. Karpe, J. R. Dickmann, and K. N. Frayn, “Fatty acids, obesity, and insulin resistance: time for a reevaluation,” Diabetes, vol. 60, no. 10, pp. 2441–2449, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. K. M. Panag, N. Kaur, and G. Goyal, “Correlation of insulin resistance by various methods with fasting insulin in obese,” International Journal of Applied and Basic Medical Research, vol. 4, no. 3, supplement 1, pp. S41–S45, 2014. View at Publisher · View at Google Scholar
  54. R. Mack, B. Skurnick, Y. Sterling-Jean, M. Pedra-Nobre, and D. Bigg, “Fasting insulin levels as a measure of insulin resistance in American blacks,” Journal of Medicine, vol. 34, no. 1–6, pp. 31–38, 2003. View at Google Scholar · View at Scopus
  55. H. B. Li, Y. R. Yang, Z. J. Mo, Y. Ding, and W. Jiang, “Silibinin improves palmitate-induced insulin resistance in C2C12 myotubes by attenuating IRS-1/PI3K/Akt pathway inhibition,” Brazilian Journal of Medical and Biological Research, vol. 48, no. 5, pp. 440–446, 2015. View at Publisher · View at Google Scholar
  56. D. Zhou, R. S. Strakovsky, X. Zhang, and Y.-X. Pan, “The skeletal muscle wnt pathway may modulate insulin resistance and muscle development in a diet-induced obese rat model,” Obesity, vol. 20, no. 8, pp. 1577–1584, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Avogaro, S. V. de Kreutzenberg, and G. P. Fadini, “Oxidative stress and vascular disease in diabetes: Is the dichotomization of insulin signaling still valid?” Free Radical Biology and Medicine, vol. 44, no. 6, pp. 1209–1215, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Guo, “Molecular basis of insulin resistance: the role of IRS and Foxo1 in the control of diabetes mellitus and its complications,” Drug Discovery Today: Disease Mechanisms, vol. 10, no. 1-2, pp. e27–e33, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Fuller, A. J. Richard, D. M. Ribnicky, R. Beyl, R. Mynatt, and J. M. Stephens, “St. John's Wort has metabolically favorable effects on adipocytes in vivo,” Evidence-Based Complementary and Alternative Medicine, vol. 2014, Article ID 862575, 8 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. E. Tomás, Y.-S. Lin, Z. Dagher et al., “Hyperglycemia and insulin resistance: possible mechanisms,” Annals of the New York Academy of Sciences, vol. 967, pp. 43–51, 2002. View at Google Scholar · View at Scopus
  61. N. M. Leguisamo, A. M. Lehnen, U. F. Machado et al., “GLUT4 content decreases along with insulin resistance and high levels of inflammatory markers in rats with metabolic syndrome,” Cardiovascular Diabetology, vol. 11, article 100, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. S.-I. Ikeda, Y. Tamura, S. Kakehi et al., “Exercise-induced enhancement of insulin sensitivity is associated with accumulation of M2-polarized macrophages in mouse skeletal muscle,” Biochemical and Biophysical Research Communications, vol. 441, no. 1, pp. 36–41, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. J. Rung, S. Cauchi, A. Albrechtsen et al., “Genetic variant near IRS1 is associated with type 2 diabetes, insulin resistance and hyperinsulinemia,” Nature Genetics, vol. 41, no. 10, pp. 1110–1115, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. S. M. Schultze, B. A. Hemmings, M. Niessen, and O. Tschopp, “PI3K/AKT, MAPK and AMPK signalling: protein kinases in glucose homeostasis,” Expert Reviews in Molecular Medicine, vol. 14, article e1, 21 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  65. R. S. Garofalo, S. J. Orena, K. Rafidi et al., “Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKBβ,” Journal of Clinical Investigation, vol. 112, no. 2, pp. 197–208, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. S. E. Leney and J. M. Tavaré, “The molecular basis of insulin-stimulated glucose uptake: Signalling, trafficking and potential drug targets,” Journal of Endocrinology, vol. 203, no. 1, pp. 1–18, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. U. Kintscher and R. E. Law, “PPARγ-mediated insulin sensitization: the importance of fat versus muscle,” The American Journal of Physiology: Endocrinology and Metabolism, vol. 288, no. 2, pp. E287–E291, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Rocchi and J. Auwerx, “Peroxisome proliferator-activated receptor gamma, the ultimate liaison between fat and transcription,” British Journal of Nutrition, vol. 84, supplement 2, pp. S223–S227, 2000. View at Publisher · View at Google Scholar · View at Scopus