Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
권호 표지
DOI QR코드

DOI QR Code

Effect of Prunetin on Streptozotocin-Induced Diabetic Nephropathy in Rats - a Biochemical and Molecular Approach

  • Jose Vinoth Raja Antony Samy (Department of Biochemistry and Biotechnology, Faculty of Science, Annamalai University) ;
  • Nirubama Kumar (Department of Biochemistry, Kongunadu Arts and Science College) ;
  • Sengottuvelu Singaravel (Department of Pharmacology, Nandha College of Pharmacy) ;
  • Rajapandiyan Krishnamoorthy (Department of Food Science and Nutrition, College of Food and Agriculture Sciences, King Saud University) ;
  • Mohammad A Alshuniaber (Department of Food Science and Nutrition, College of Food and Agriculture Sciences, King Saud University) ;
  • Mansour K. Gatasheh (Department of Biochemistry, College of Science, King Saud University) ;
  • Amalan Venkatesan (Department of Biochemistry and Biotechnology, Faculty of Science, Annamalai University) ;
  • Vijayakumar Natesan (Department of Biochemistry and Biotechnology, Faculty of Science, Annamalai University) ;
  • Sung-Jin Kim (Department of Pharmacology and Toxicology, Metabolic Diseases Research Laboratory, School of Dentistry, Kyung Hee University)
  • Received : 2023.03.27
  • Accepted : 2023.07.30
  • Published : 2023.11.01
Download PDF
⟨ Previous Next ⟩

Abstract

In the modern era, chronic kidney failure due to diabetes has spread across the globe. Prunetin (PRU), a component of herbal medicines, has a broad variety of pharmacological activities; these may help to slow the onset of diabetic kidney disease. The anti-nephropathic effects of PRU have not yet been reported. The present study explored the potential nephroprotective actions of PRU in diabetic rats. For 28 days, nephropathic rats were given oral doses of PRU (20, 40, and 80 mg/kg). Body weight, blood urea, creatinine, total protein, lipid profile, liver marker enzymes, carbohydrate metabolic enzymes, C-reactive protein, antioxidants, lipid peroxidative indicators, and the expression of insulin receptor substrate 1 (IRS-1) and glucose transporter 2 (GLUT-2) mRNA genes were all examined. Histological examinations of the kidneys, liver, and pancreas were also performed. The oral treatment of PRU drastically lowered the blood glucose, HbA1c, blood urea, creatinine, serum glutamic-oxaloacetic transaminase, serum glutamic pyruvic transaminase, alkaline phosphatase, lipid profile, and hexokinase. Meanwhile, the levels of fructose 1,6-bisphosphatase, glucose-6-phosphatase, and phosphoenol pyruvate carboxykinase were all elevated, but glucose-6-phosphate dehydrogenase dropped significantly. Inflammatory marker antioxidants and lipid peroxidative markers were also less persistent due to this administration. PRU upregulated the IRS-1 and GLUT-2 gene expression in the nephropathic group. The possible renoprotective properties of PRU were validated by histopathology of the liver, kidney, and pancreatic tissues. It is therefore proposed that PRU (80 mg/kg) has considerable renoprotective benefits in diabetic nephropathy in rats.

Keywords

Acknowledgement

The authors acknowledge the support from the Researchers supporting project number (RSP2023R393), King Saud University, Riyadh, Saudi Arabia.

References

  1. Aebi, H. (1984) Catalase in vitro. Methods Enzymol. 105, 121-126. https://doi.org/10.1016/S0076-6879(84)05016-3
  2. Alaofi, A. L. (2020) Sinapic acid ameliorates the progression of streptozotocin (STZ)-induced diabetic nephropathy in rats via NRF2/HO-1 mediated pathways. Front. Pharmacol. 11, 1119.
  3. Amalan, V., Vijayakumar, N. and Ramakrishnan, A. (2015) p-Coumaric acid regulates blood glucose and antioxidant levels in streptozotocin-induced diabetic rats. J. Chem. Pharm. Res. 7, 831-839.
  4. Amalan, V., Jose Vinoth Raja, A., Rajeswari, R., Jayaprakash, R. and Vijayakumar, N. (2021) Antithrombotic, antihemolytic activities and protein conjugation properties of silver nanoparticles synthesized from Turbinaria ornata. Asian J. Chem. 33, 1736-1742. https://doi.org/10.14233/ajchem.2021.23237
  5. Amalan, V. and Vijayakumar, N. (2015) Antihyperglycemic effect of p-coumaric acid on streptozotocin induced diabetic rats. Indian J. Appl. Res. 5, 10-13.
  6. Amalan, V., Vijayakumar, N., Indumathi, D. and Ramakrishnan, A. (2016) Antidiabetic and antihyperlipidemic activity of p-coumaric acid in diabetic rats, role of pancreatic GLUT 2: in vivo approach. Biomed. Pharmacother. 84, 230-236. https://doi.org/10.1016/j.biopha.2016.09.039
  7. Asmat, U., Abad, K. and Ismail, K. (2016) Diabetes mellitus and oxidative stress-a concise review. Saudi Pharm. J. 24, 547-553. https://doi.org/10.1016/j.jsps.2015.03.013
  8. Bancroft, J. D., Stevens, A. and Turner, D. R. (1996) Theory and Practice of Histological Techniques, 4th ed. Churchill Livingstone, New York, London, San Francisco, Tokyo.
  9. Barnes, S. (2004) Soy isoflavones-phytoestrogens and what else? J. Nutr. 134, 1225-1228. https://doi.org/10.1093/jn/134.5.1225S
  10. Bastaki, S. (2005) Diabetes mellitus and its treatment. Int. J. Diabetes Metab. 13, 111-134.
  11. Berry, G. T., Baynes, J. W., Wells-Knecht, K. J., Szwergold, B. S. and Santer, R. (2005) Elements of diabetic nephropathy in a patient with GLUT2 deficiency. Mol. Genet. Metab. 8, 473-477.
  12. Bisse, E. and Abraham, E. C. (1985) New less temperature sensitive, micro chromatographic method for the separation and quantitation of glycosylated hemoglobin using a noncyanide buffer system. J. Chromatogr. 344, 81-91. https://doi.org/10.1016/S0378-4347(00)82009-5
  13. Boura-Halfon, S. and Zick, Y. (2009) Phosphorylation of IRS proteins, insulin action, and insulin resistance. Am. J. Physiol. Endocrinol. Metab. 296, 581-591.
  14. Brenna, O., Qvigstad, G., Brenna, E. and Waldum, H. L. (2003) Cytotoxicity of streptozotocin on neuroendocrine cells of the pancreas and the gut. Dig. Dis. Sci. 48, 906-910. https://doi.org/10.1023/A:1023043411483
  15. Burgi, W., Briner, M., Franken, N. and Kessler, A. C. (1988) One-step sandwich enzyme immunoassay for insulin using monoclonal antibodies. Clin. Biochem. 21, 311-314. https://doi.org/10.1016/S0009-9120(88)80087-0
  16. Cheng, D., Liang, B. and Li, Y. (2013) Antihyperglycemic effect of Ginkgo biloba extract in streptozotocin-induced diabetes in rats. Biomed. Res. Int. 2013, 162724.
  17. Dal, S. and Sigrist, S. (2016) The protective effect of antioxidants consumption on diabetes and vascular complications. Diseases 4, 24.
  18. Diaz-Flores, M., Ibanez-Hernandez, M. A., Galvan, R. E., Gutierrez, M., Duran-Reyes, G., Medina-Navarro, R., Pascoe-Lira, D., Ortega-Camarillo, C., Vilar-Rojas, C., Cruz, M. and Baiza-Gutman, L. A. (2006) Glucose-6-phosphate dehydrogenase activity and NADPH/NADP+ ratio in liver and pancreas are dependent on the severity of hyperglycemia in rat. Life Sci. 78, 2601-2617. https://doi.org/10.1016/j.lfs.2005.10.022
  19. Duraisamy, S., Vijayakumar, N., Rajendran, J., Venkatesan, A., Kartha, B., Kandasamy, S. P., Nicoletti, M., Alharbi, N. S., Kadaikunnan, S., Khaled, J. M. and Govindarajan, M. (2022) Facile synthesis of silver nanoparticles using the Simarouba glauca leaf extract and their impact on biological outcomes: a novel perspective for nano-drug development. J. Drug Deliv. Sci. Technol. 69, 103160.
  20. Forbes, J. M. and Cooper, M. E. (2013) Mechanisms of diabetic complications. Physiol. Rev. 93, 137-188. https://doi.org/10.1152/physrev.00045.2011
  21. Gandhi, G. R., Ignacimuthu, S. and Paulraj, M. G. (2011) Solanum torvum Swartz. fruit containing phenolic compounds shows antidiabetic and antioxidant effects in streptozotocin-induced diabetic rats. Food Chem. Toxicol. 49, 2725-2733. https://doi.org/10.1016/j.fct.2011.08.005
  22. Ghorbani, A. (2017) Mechanisms of antidiabetic effects of flavonoid rutin. Biomed. Pharmacother. 96, 305-312. https://doi.org/10.1016/j.biopha.2017.10.001
  23. Giacco, F. and Brownlee, M. (2010) Oxidative stress and diabetic complications. Circ. Res. 107, 1058-1070. https://doi.org/10.1161/CIRCRESAHA.110.223545
  24. Gomes, I., Porto, M. L., Santos, M. C. L., Campagnaro, B. P., Pereira, T., Meyrelles, S. S. and Vasquez, E. C. (2014) Renoprotective, anti-oxidative and anti-apoptotic effects of oral low-dose quercetin in the C57BL/6J model of diabetic nephropathy. Lipids Health Dis. 13, 184.
  25. Haneda, M. (2006) Mechanisms for the development and progression of diabetic nephropathy. Nippon Rinsho 64 Suppl 2, 427-432.
  26. Hong, J. N., Li, W. W., Wang, L. L., Guo, H., Jiang, Y., Gao, Y. J., Tu, P. F. and Wang, X. M. (2017) Jiangtang decoction ameliorate diabetic nephropathy through the regulation of PI3K/Akt-mediated NF-κB pathways in KK-Ay mice. Chin. Med. 12, 13.
  27. Ito, F., Sono, Y. and Ito, T. (2019) Measurement and clinical significance of lipid peroxidation as a biomarker of oxidative stress: oxidative stress in diabetes, atherosclerosis, and chronic inflammation. Antioxidants 8, 72.
  28. Jadhav, V. B. and Vaghela, J. S. (2022) Sphaeranthus indicus Linn ameliorates streptozotocin-induced experimental diabetic neuropathy by targeting oxidative stress-mediated alterations. Futur. J. Pharm. Sci. 8, 55.
  29. Jiang, Z. Y., Hunt, J. V., Wolff, S. P. (1992) Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low-density lipoprotein. Anal. Biochem. 202, 384-387. https://doi.org/10.1016/0003-2697(92)90122-N
  30. Kahn, S. E. (2001) The importance of β-cell failure in the development and progression of type 2 diabetes. J. Clin. Endocrinol. Metab. 86, 4047-4058.
  31. Karalliedde, J. and Gnudi, L. (2016) Diabetes mellitus, a complex and heterogeneous disease, and the role of insulin resistance as a determinant of diabetic kidney disease. Nephrol. Dial. Transplant. 31, 206-213.
  32. Kooptiwut, S., Samon, K., Semprasert, N., Suksri., K. and Yenchitsomanus, P. T. (2020) Prunetin protects against dexamethasone-induced pancreatic B-cell apoptosis via modulation of p53 signaling pathway. Nat. Prod. Commun. 15, doi: 10.1177/1934578X20916328.
  33. Lopez-Novoa, J. M., Rodriguez-Pena, A. B., Ortiz, A., Martinez-Salgado, C. and Lopez Hernandez F. J. (2011) Etiopathology of chronic tubular, glomerular and renovascular nephropathies: clinical implications. J. Transl. Med. 9, 13.
  34. Manogar, P., Morvinyabesh, J. E., Ramesh, P., Jeyaleela, G. D., Amalan, V., Ajarem, J. S., Allam, A. A., Khim, J. S. and Vijayakumar, N. (2022) Biosynthesis and antimicrobial activity of aluminium oxide nanoparticles using Lyngbya majuscula extract. Mater. Lett. 311, 131569.
  35. Marklund, S. and Marklund, G. (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 47, 469-474. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
  36. Mestry, S. N., Dhodi, J. B., Kumbhar, S. B. and Juvekar, A. R. (2017) Attenuation of diabetic nephropathy in streptozotocin-induced diabetic rats by Punica granatum Linn. leaves extract. J. Tradit. Complement. 7, 273-280. https://doi.org/10.1016/j.jtcme.2016.06.008
  37. Moron, M. S., Depierre, J. W. and Mannervik, B. (1979) Levels of glutathione, glutathione reductase and glutathione-s-transferase activities in rat lung and liver. Biochim. Biophys. Acta 582, 67-78. https://doi.org/10.1016/0304-4165(79)90289-7
  38. Mutalik, S., Sulochana, B., Chetana, M., Udupa, N. and Devi, P. U. (2003) Preliminary studies on acute and subacute toxicity of an antidiabetic herbal preparation-Dianex. Indian J. Exp. Biol. 41, 316-320.
  39. Natesan, V., Mani, R. and Arumugam, R. (2016) Clinical aspects of urea cycle dysfunction and altered brain energy metabolism on modulation of glutamate receptors and transporters in acute and chronic hyperammonemia. Biomed. Pharmacother. 81, 192-202. https://doi.org/10.1016/j.biopha.2016.04.010
  40. Nesbitt, K. N. (2004) An overview of diabetic nephropathy. J. Pharm. Prac. 17, 75-79. https://doi.org/10.1177/0897190003261312
  41. Park, S., Lim, W., Bazer, F. W., Whang, K. Y. and Song, G. (2019) Quercetin inhibits proliferation of endometriosis regulating cyclin D1 and its target microRNAs in vitro and in vivo. J. Nutr. Biochem. 63, 87-100. https://doi.org/10.1016/j.jnutbio.2018.09.024
  42. Pasaoglu, H., Sancak, B. and Bukan, N. (2004) Lipid peroxidation and resistance to oxidation in patients with type 2 diabetes mellitus. Tohoku J. Exp. Med. 203, 211-218. https://doi.org/10.1620/tjem.203.211
  43. Peers, C., Paffett, M. L. and Walker, B. R. (2007) Vascular adaptations to hypoxia: molecular and cellular mechanisms regulating vascular tone. Essays Biochem. 43, 105-120. https://doi.org/10.1042/bse0430105
  44. Sharma, D., Gondaliya, P., Tiwari, V. and Kalia, K. (2019) Kaempferol attenuates diabetic nephropathy by inhibiting RhoA/Rho-kinase mediated inflammatory signaling. Biomed. Pharmacother. 109, 1610-1619. https://doi.org/10.1016/j.biopha.2018.10.195
  45. Sharma, S., Kulkarni, S. K. and Chopra, K. (2006) Curcumin, the active principle of turmeric (Curcuma longa), ameliorates diabetic nephropathy in rats. Clin. Exp. Pharmacol. Physiol. 33, 940-945. https://doi.org/10.1111/j.1440-1681.2006.04468.x
  46. Shi, G. J., Li, Y., Cao, Q. H., Wu, H. X., Tang, X. Y., Gao, X. H., Yu, J. Q., Chen, Z. and Yang, Y. (2019) In vitro and in vivo evidence that quercetin protects against diabetes and its complications: a systematic review of the literature. Biomed. Pharmacother. 109, 1085-1099. https://doi.org/10.1016/j.biopha.2018.10.130
  47. Sivakumar, S., Palsamy, P. and Subramanian, S. P. (2010) Impact of D-pinitol on the attenuation of proinflammatory cytokines, hyperglycemia-mediated oxidative stress and protection of kidney tissue ultrastructure in streptozotocin-induced diabetic rats. Chem. Biol. Interact. 188, 237-245. https://doi.org/10.1016/j.cbi.2010.07.014
  48. Stefano, G. B., Challenger, S. and Kream, R. M. (2016) Hyperglycemia-associated alterations in cellular signaling and dysregulated mitochondrial bioenergetics in human metabolic disorders. Eur. J. Nutr. 55, 2339-2345. https://doi.org/10.1007/s00394-016-1212-2
  49. Thomasset, S. C., Berry, D. P., Garcea, G., Marczylo, T., Steward, W. P. and Gescher, A. J. (2007) Dietary polyphenolic phytochemicals-promising cancer chemopreventive agents in humans? A review of their clinical properties. Int. J. Cancer 120, 451-458. https://doi.org/10.1002/ijc.22419
  50. Townsend, D. M., Tew, K. D. and Tapiero, H. (2003) The importance of glutathione in human disease. Biomed. Pharmacother. 57, 145-155. https://doi.org/10.1016/S0753-3322(03)00043-X
  51. Trinder, P. (1969) Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann. Clin. Biochem. 6, 24.
  52. Venkatesan, A., Roy, A., Kulandaivel, S., Natesan, V. and Kim, S. J. (2022) p-Coumaric acid nanoparticles ameliorate diabetic nephropathy via regulating mRNA expression of KIM-1 and GLUT-2 in streptozotocin-induced diabetic rats. Metabolites 12, 1166.
  53. Viberti, G. and Walker, J. D. (1991) Natural history and pathogenesis of diabetic nephropathy. J. Diabetes Complicat. 5, 72-75. https://doi.org/10.1016/0891-6632(91)90022-H
  54. Vinayagam, R. and Xu, B. (2015) Antidiabetic properties of dietary flavonoids: a cellular mechanism review. Nutr. Metab. 12, 60.
  55. Wang, G. G., Lu, X. H., Li, W., Zhao, X. and Zhang, C. (2011) Protective effects of luteolin on diabetic nephropathy in STZ-induced diabetic rats. Evid. Based Complement. Alternat. Med. 2011, 323171.
  56. Wang, T., Wang, J., Hu, X., Huang, X. J. and Chen, G. X. (2020) Current understanding of glucose transporter 4 expression and functional mechanisms. World J. Biol. Chem. 11, 76-98. https://doi.org/10.4331/wjbc.v11.i3.76
  57. Yang, G., Ham, I. and Choi, H. Y. (2013) Anti-inflammatory effect of prunetin via the suppression of NF-κB pathway. Food Chem. Toxicol. 58, 124-132. https://doi.org/10.1016/j.fct.2013.03.039
  58. You, Y. K., Huang, X. R., Chen, H. Y., Lyu, X. F., Liu, H. F. and Lan, H. Y. (2016) C-reactive protein promotes diabetic kidney disease in db/db mice via the CD32b-Smad3-mTOR signaling pathway. Sci. Rep. 6, 26740.
  59. Zhang, Y., Lu, X., Hong, J., Chao, M., Gu, W., Wang, W. and Ning, G. (2010) Positive correlations of liver enzymes with metabolic syndrome including insulin resistance in newly diagnosed type 2 diabetes mellitus. Endocrine 38, 181-187. https://doi.org/10.1007/s12020-010-9369-6