Location via proxy:   [ UP ]  
[Report a bug]   [Manage cookies]                
Skip to main content

Advertisement

Springer Nature Link
Log in

Anti-Diabetic and Anti-Nephritic Activities of Grifola frondosa Mycelium Polysaccharides in Diet-Streptozotocin-Induced Diabetic Rats Via Modulation on Oxidative Stress

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Grifola frondosa is an edible fungus with a variety of potential pharmacological activities. This study investigates the hypoglycemic, anti-diabetic nephritic, and antioxidant properties of G. frondosa polysaccharides in diet-streptozotocin-induced diabetic rats. After a 4-week treatment with 100 mg/kg of metformin and 200 mg/kg of one of four different G. frondosa polysaccharide mixtures (especially GFPS3 and GFPS4), diabetic rats had enhanced body weight and suppressed plasma glucose, indicating the hypoglycemic activities of the G. frondosa polysaccharides. G. frondosa polysaccharides regulated the level of serum creatinine, blood urea nitrogen, N-acetyl-β-d-glucosaminidase, and albuminuria; inhibited the serum levels of interleukin (IL)-2, IL-6, and TNF-α; and enhanced the serum levels of matrix metalloproteinase 9 and interferon-α, confirming their anti-diabetic nephritic activities. G. frondosa polysaccharides ameliorated the pathological alterations in the kidneys of diabetic rats. Moreover, G. frondosa polysaccharides modulated the serum levels of oxidant factors such as superoxide dismutase, glutathione peroxidase, catalase, malondialdehyde, and reactive oxygen species, revealing their antioxidant properties. Furthermore, the administration of G. frondosa polysaccharides inhibited nuclear factor kappa B activities in the serum and kidneys. All of the data revealed that the activation of nuclear factor kappa B plays a central role in G. frondosa polysaccharide-mediated anti-diabetic and anti-nephritic activities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Sheikh, B. A., Pari, L., Rathinam, A., & Chandramohan, R. (2015). Trans-anethole, a terpenoid ameliorates hyperglycemia by regulating key enzymes of carbohydrate metabolism in streptozotocin induced diabetic rats. Biochimie, 112, 57–65.

    Article  CAS  PubMed  Google Scholar 

  2. Kerner, W., & Bruckel, J. (2014). Definition, classification and diagnosis of diabetes mellitus. Experimental and Clinical Endocrinology & Diabetes, 122(7), 384–386.

    Article  CAS  Google Scholar 

  3. Putakala, M., Gujjala, S., Nukala, S., & Desireddy, S. (2017). Beneficial effects of Phyllanthus amarus against high fructose diet induced insulin resistance and hepatic oxidative stress in male Wistar rats. Applied Biochemistry and Biotechnology, 183(3), 744–764.

    Article  CAS  PubMed  Google Scholar 

  4. Jiang, P., Dong, Z., Ma, B., Ni, Z., Duan, H., Li, X., Wang, B., Ma, X., Wei, Q., Ji, X., & Li, M. (2016). Effect of Vanadyl rosiglitazone, a new insulin-mimetic vanadium complexes, on glucose homeostasis of diabetic mice. Applied Biochemistry and Biotechnology, 180(5), 841–851.

    Article  CAS  PubMed  Google Scholar 

  5. Zhu, K., Kakehi, T., Matsumoto, M., Iwata, K., Ibi, M., Ohshima, Y., Zhang, J., Liu, J., Wen, X., Taye, A., Fan, C., Katsuyama, M., Sharma, K., & Yabe-Nishimura, C. (2015). NADPH oxidase NOX1 is involved in activation of protein kinase C and premature senescence in early stage diabetic kidney. Free Radical Biology & Medicine, 83, 21–30.

    Article  CAS  Google Scholar 

  6. Fornoni, A., Ijaz, A., Tejada, T., & Lenz, O. (2008). Role of inflammation in diabetic nephropathy. Current Diabetes Reviews, 4(1), 10–17.

    Article  CAS  PubMed  Google Scholar 

  7. Yuan, H. D., Huang, B., & Chung, S. H. (2011). Protective effect of cinnamaldehyde on streptozotocin-induced damage in rat pancreatic β-cells. Food Science and Biotechnology, 20(5), 1271–1276.

    Article  CAS  Google Scholar 

  8. Elsherbiny, N. M., El-Sherbiny, M., & Said, E. (2015). Amelioration of experimentally induced diabetic nephropathy and renal damage by nilotinib. Journal of Physiology and Biochemistry, 71(4), 635–648.

    Article  CAS  PubMed  Google Scholar 

  9. Wu, J. Q., Kosten, T. R., & Zhang, X. Y. (2013). Free radicals, antioxidant defense systems, and schizophrenia. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 46, 200–206.

    Article  CAS  Google Scholar 

  10. Khatiwala, R. V., Zhang, S., Li, X., Devejian, N., Bennett, E. and Cai, C. (2018) Inhibition of p16(INK4A) to rejuvenate aging human cardiac progenitor cells via the upregulation of anti-oxidant and NFkappaB signal pathways. Stem cell reviews.

  11. Suryavanshi, S. V., & Kulkarni, Y. A. (2017). NF-κβ: a potential target in the management of vascular complications of diabetes. Frontiers in Pharmacology, 8.

  12. Kania, D. S., Gonzalvo, J. D., & Weber, Z. A. (2011). Saxagliptin: a clinical review in the treatment of type 2 diabetes mellitus. Clinical Therapeutics, 33(8), 1005–1022.

    Article  CAS  PubMed  Google Scholar 

  13. Scheen, A. (2007). Antidiabetic agents in subjects with mild dysglycaemia: prevention or early treatment of type 2 diabetes? Diabetes & Metabolism, 33(1), 3–12.

    Article  CAS  Google Scholar 

  14. Salihu Shinkafi, T., Bello, L., Wara Hassan, S., & Ali, S. (2015). An ethnobotanical survey of antidiabetic plants used by Hausa-Fulani tribes in Sokoto, Northwest Nigeria. Journal of Ethnopharmacology, 172, 91–99.

    Article  PubMed  Google Scholar 

  15. Liu, C., Song, J., Teng, M., Zheng, X., Li, X., Tian, Y., Pan, M., Li, Y., Lee, R. J., & Wang, D. (2016). Antidiabetic and antinephritic activities of aqueous extract of Cordyceps militaris fruit body in diet-streptozotocin-induced diabetic Sprague Dawley rats. Oxidative Medicine and Cellular Longevity, 2016, 9685257.

    PubMed  PubMed Central  Google Scholar 

  16. Liu, C., Zeng, X., Li, Y., Ma, H., Song, J., Li, Y., Zhou, Y., Lee, R. J., & Wang, D. (2017). Investigation of hypoglycemic, hypolipidemic and antinephritic activities of Paecilomyces tenuipes N45 in diet/streptozotocin induced diabetic rats. Molecular Medicine Reports, 15(5), 2807–2813.

    Article  CAS  PubMed  Google Scholar 

  17. Du, L., Liu, C., Teng, M., Meng, Q., Lu, J., Zhou, Y., Liu, Y., Cheng, Y., Wang, D., & Teng, L. (2016). Anti-diabetic activities of Paecilomyces tenuipes N45 extract in alloxan-induced diabetic mice. Molecular Medicine Reports, 13(2), 1701–1708.

    Article  CAS  PubMed  Google Scholar 

  18. He, X., Wang, X., Fang, J., Chang, Y., Ning, N., Guo, H., Huang, L., Huang, X., & Zhao, Z. (2017). Polysaccharides in Grifola frondosa mushroom and their health promoting properties: a review. International Journal of Biological Macromolecules, 101, 910–921.

    Article  CAS  PubMed  Google Scholar 

  19. Kubo, K., & Nanba, H. (1997). Anti-hyperliposis effect of maitake fruit body (Grifola frondosa). I. Biological & Pharmaceutical Bulletin, 20(7), 781–785.

    Article  CAS  Google Scholar 

  20. Hong, L., Xun, M., & Wutong, W. (2007). Anti-diabetic effect of an alpha-glucan from fruit body of maitake (Grifola frondosa) on KK-ay mice. The Journal of Pharmacy and Pharmacology, 59(4), 575–582.

    Article  CAS  PubMed  Google Scholar 

  21. Chen, Z., Tang, Y., Liu, A., Jin, X., Zhu, J., & Lu, X. (2017). Oral administration of Grifola frondosa polysaccharides improves memory impairment in aged rats via antioxidant action. Molecular Nutrition & Food Research, 61(11).

  22. Zhu, H., Sheng, K., Yan, E., Qiao, J., & Lv, F. (2012). Extraction, purification and antibacterial activities of a polysaccharide from spent mushroom substrate. International Journal of Biological Macromolecules, 50(3), 840–843.

    Article  CAS  PubMed  Google Scholar 

  23. Song, J., Wang, Y., Liu, C., Huang, Y., He, L., Cai, X., Lu, J., Liu, Y., & Wang, D. (2016). Cordyceps militaris fruit body extract ameliorates membranous glomerulonephritis by attenuating oxidative stress and renal inflammation via the NF-kappaB pathway. Food & Function, 7(4), 2006–2015.

    Article  CAS  Google Scholar 

  24. Cui, H., Chen, Y., Wang, S., Kai, G., & Fang, Y. (2011). Isolation, partial characterisation and immunomodulatory activities of polysaccharide from Morchella esculenta. Journal of the Science of Food and Agriculture, 91(12), 2180–2185.

    CAS  PubMed  Google Scholar 

  25. Dong, Y., Jing, T., Meng, Q., Liu, C., Hu, S., Ma, Y., Liu, Y., Lu, J., Cheng, Y., Wang, D., & Teng, L. (2014). Studies on the antidiabetic activities of Cordyceps militaris extract in diet-streptozotocin-induced diabetic Sprague-Dawley rats. BioMed Research International, 2014, 160980.

    PubMed  PubMed Central  Google Scholar 

  26. Wang, J., Song, J., Wang, D., Zhang, N., Lu, J., Meng, Q., Zhou, Y., Wang, N., Liu, Y., Wang, D., & Teng, L. (2016). The anti-membranous glomerulonephritic activity of purified polysaccharides from Irpex lacteus Fr. International Journal of Biological Macromolecules, 84, 87–93.

    Article  CAS  PubMed  Google Scholar 

  27. Williams, M. E. (2005). Diabetic nephropathy: the proteinuria hypothesis. American Journal of Nephrology, 25(2), 77–94.

    Article  PubMed  Google Scholar 

  28. Rubattu, S., Pagliaro, B., Pierelli, G., Santolamazza, C., Castro, S. D., Mennuni, S., & Volpe, M. (2014). Pathogenesis of target organ damage in hypertension: role of mitochondrial oxidative stress. International Journal of Molecular Sciences, 16(1), 823–839.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Mahendran, G., Thamotharan, G., Sengottuvelu, S., & Bai, V. N. (2014). Anti-diabetic activity of Swertia corymbosa (Griseb.) Wight ex C.B. Clarke aerial parts extract in streptozotocin induced diabetic rats. Journal of Ethnopharmacology, 151(3), 1175–1183.

    Article  CAS  PubMed  Google Scholar 

  30. Ellis, E. N., & Good, B. H. (1991). Prevention of glomerular basement membrane thickening by aminoguanidine in experimental diabetes mellitus. Metabolism, 40(10), 1016–1019.

    Article  CAS  PubMed  Google Scholar 

  31. Hua, W., Huang, H. Z., Tan, L. T., Wan, J. M., Gui, H. B., Zhao, L., Ruan, X. Z., Chen, X. M., & Du, X. G. (2015). CD36 mediated fatty acid-induced podocyte apoptosis via oxidative stress. PLoS One, 10(5), e0127507.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Rolo, A. P., & Palmeira, C. M. (2006). Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicology and Applied Pharmacology, 212(2), 167–178.

    Article  CAS  PubMed  Google Scholar 

  33. Tang, Z., Gao, H., Wang, S., Wen, S., & Qin, S. (2013). Hypolipidemic and antioxidant properties of a polysaccharide fraction from Enteromorpha prolifera. International Journal of Biological Macromolecules, 58, 186–189.

    Article  CAS  PubMed  Google Scholar 

  34. Lo, C. S., Shi, Y. X., Chenier, I., Ghosh, A., Wu, C. H., Cailhier, J. F., Ethier, J., Lattouf, J. B., Filep, J. G., Ingelfinger, J. R., Zhang, S. L., & Chan, J. S. D. (2017). Heterogeneous nuclear ribonucleoprotein F stimulates Sirtuin-1 gene expression and attenuates nephropathy progression in diabetic mice. Diabetes, 66(7), 1964–1978.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Sebai, H., Selmi, S., Rtibi, K., Souli, A., Gharbi, N., & Sakly, M. (2013). Lavender (Lavandula stoechas L.) essential oils attenuate hyperglycemia and protect against oxidative stress in alloxan-induced diabetic rats. Lipids in Health and Disease, 12(1), 189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bertelli, R., Di Donato, A., Cioni, M., Grassi, F., Ikehata, M., Bonanni, A., Rastaldi, M. P., & Ghiggeri, G. M. (2014). LPS nephropathy in mice is ameliorated by IL-2 independently of regulatory T cells activity. PLoS One, 9(10), e111285.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Peters, T., Bloch, W., Wickenhauser, C., Tawadros, S., Oreshkova, T., Kess, D., Krieg, T., Muller, W., & Scharffetter-Kochanek, K. (2006). Terminal B cell differentiation is skewed by deregulated interleukin-6 secretion in beta2 integrin-deficient mice. Journal of Leukocyte Biology, 80(3), 599–607.

    Article  CAS  PubMed  Google Scholar 

  38. Eilenberg, W., Stojkovic, S., Piechota-Polanczyk, A., Kaider, A., Kozakowski, N., Weninger, W. J., Nanobachvili, J., Wojta, J., Huk, I., Demyanets, S., & Neumayer, C. (2017). Neutrophil gelatinase associated lipocalin (NGAL) is elevated in type 2 diabetics with carotid artery stenosis and reduced under metformin treatment. Cardiovascular Diabetology, 16(1), 98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Li, S., Zhang, Y., & Zhao, J. (2007). Preparation and suppressive effect of astragalus polysaccharide in glomerulonephritis rats. International Immunopharmacology, 7(1), 23–28.

    Article  CAS  PubMed  Google Scholar 

  40. Zhang, S., Xin, H., Li, Y., Zhang, D., Shi, J., Yang, J., & Chen, X. (2013). Skimmin, a coumarin from Hydrangea paniculata, slows down the progression of membranous glomerulonephritis by anti-inflammatory effects and inhibiting immune complex deposition. Evidence-based complementary and alternative medicine. eCAM, 2013, 819296.

  41. Pan, P., Wang, Y. J., Han, L., Liu, X., Zhao, M., & Yuan, Y. F. (2010). Effects of sodium houttuyfonate on expression of NF-kappaB and MCP-1 in membranous glomerulonephritis. Journal of Ethnopharmacology, 131(1), 203–209.

    Article  CAS  PubMed  Google Scholar 

  42. Manna, P., Das, J., Ghosh, J., & Sil, P. C. (2010). Contribution of type 1 diabetes to rat liver dysfunction and cellular damage via activation of NOS, PARP, IkappaBalpha/NF-kappaB, MAPKs, and mitochondria-dependent pathways: prophylactic role of arjunolic acid. Free Radical Biology & Medicine, 48(11), 1465–1484.

    Article  CAS  Google Scholar 

  43. Rashid, S., Nafees, S., Siddiqi, A., Vafa, A., Afzal, S. M., Parveen, R., Ali, N., Hasan, S. K., Barnwal, P., Shahid, A., & Sultana, S. (2017). Partial protection by 18beta glycrrhetinic acid against cisplatin induced oxidative intestinal damage in Wistar rats: possible role of NFkB and caspases. Pharmacological Reports : PR, 69(5), 1007–1013.

    Article  CAS  PubMed  Google Scholar 

  44. Oh, S. W., Lee, Y. M., Kim, S., Chin, H. J., Chae, D. W., & Na, K. Y. (2014). Cobalt chloride attenuates oxidative stress and inflammation through NF-kappaB inhibition in human renal proximal tubular epithelial cells. Journal of Korean Medical Science, 29(Suppl 2), S139–S145.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Methacanon, P., Madla, S., Kirtikara, K., & Prasitsil, M. (2005). Structural elucidation of bioactive fungi-derived polymers. Carbohydrate Polymers, 60(2), 199–203.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work is supported by the Project from Health and Family Planning Commission Project from Jiangsu province (no. H201536) and Scientific Research Program of the Affiliated Hospital of Jiangsu University in China (no. jdfyRC-2015004).

Author information

Authors and Affiliations

  1. Affiliated Hospital of Jiangsu University, Jiangsu University, Zhenjiang, 212001, China

    Ling Kou, Mingzhao Du, Peijing Liu, Baohai Zhang, Ping Yang, Mengyuan Shang & Xiaodong Wang

  2. Department of Neurology, the Second Hospital of Jilin University, Jilin University, Changchun, 130041, China

    Yizhi Zhang

Authors
  1. Ling Kou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mingzhao Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peijing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Baohai Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yizhi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ping Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mengyuan Shang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiaodong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mingzhao Du.

Ethics declarations

Conflict of Interest

The authors have declared that there is no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kou, L., Du, M., Liu, P. et al. Anti-Diabetic and Anti-Nephritic Activities of Grifola frondosa Mycelium Polysaccharides in Diet-Streptozotocin-Induced Diabetic Rats Via Modulation on Oxidative Stress. Appl Biochem Biotechnol 187, 310–322 (2019). https://doi.org/10.1007/s12010-018-2803-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-018-2803-6

Keywords

Search

Navigation