Ameliorative effects of histidine on oxidative stress, tumor necrosis factor alpha (TNF-α), and renal histological alterations in streptozotocin/nicotinamide-induced type 2 diabetic rats

Document Type: Original Article

Authors

1 Department of Biochemistry and Genetics, Lorestan University of Medical Sciences, Khorramabad, Iran

2 Growth and Development Research Center, Tehran University of Medical Science, Tehran, Iran

3 Department of Clinical Biochemistry, Faculty of Medicine, Ardabil University of Medical Sciences, Ardabil, Iran

4 Department of Clinical Biochemistry, School of Medicine, Student Research Committee, Shahid Beheshti University of Medical Sciences, Tehran, Iran

5 Department of Clinical Biochemistry, Faculty of Medicine, Lorestan University of Medical Sciences, Khorramabad, Iran

6 Agricultural and Natural Resources Research and Education Center, Department of Animal Science, Lorestan, Iran

7 Nutritional Health Research Center, Lorestan University of Medical Sciences, Khorramabad, Iran

8 Razi Herbal Medicines Research Center, Faculty of Medicine, Lorestan University of Medical Sciences, Khorramabad, Iran

Abstract

Objective(s): The present study sought to evaluate the beneficial effects of histidine (His) on oxidative stress, tumor necrosis factor alpha (TNF-α), renal histological alterations and anti-oxidant enzymes gene expressions in type 2 diabetic rats.
Materials and Methods: Streptozotocin/nicotinamide (STZ/NA) induced diabetic rats were used as an animal model of type 2 diabetes. One group of rats received daily His (1000 mg/l) in drinking water for 8 weeks, whereas other groups (control and untreated diabetic groups) received only water. Different parameters such as glucose, insulin, insulin resistance, lipid profile, cardiac risk ratios, renal functional markers, and oxidative stress were determined in all groups. Moreover, renal histological alterations, mRNA expressions of anti-oxidant enzymes, and TNF-α were evaluated in the rats.
Results: His exhibited a protective effect on glucose, insulin, insulin resistance, lipid profile, cardiac risk ratios, renal functional markers, oxidative stress, and TNF-α. Furthermore, His restored the renal histological alterations and normalized the augmented mRNA expressions of renal anti-oxidant enzymes (glutathione peroxidase (GPX) and Cu-Zn superoxide dismutase (Cu-Zn SOD)) and TNF-α.
Conclusion: His could ameliorate diabetes complications related to oxidative stress, inflammation, dyslipidemia, hyperglycemia, insulin resistance, and nephropathy. Hence, the use of this amino acid is recommended for diabetic patients in order to reduce diabetes complications.

Keywords


1. Chen L, Magliano DJ, Zimmet PZ. The worldwide epidemiology of type 2 diabetes mellitus--present and future perspectives. Nat Rev Endocrinol 2011; 8:228-236.
2. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 2014; 103:137-149.
3. Hajivandi A, Amiri M. World diabetes day 2013: diabetes mellitus and nephrology. J nephropharmacol 2013; 2:31-32.
4. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001; 414:813-820.
5. Amiri M. Oxidative stress and free radicals in liver and kidney diseases; an updated short-review. J Nephropathol 2018; 7.
6. Rodrigo R, Bosco C. Oxidative stress and protective effects of polyphenols: comparative studies in human and rodent kidney. A review. Comp Biochem Physiol C Toxicol Pharmacol 2006; 142:317-327.
7. Shin AH, Oh CJ, Park JW. Glycation-induced inactivation of anti-oxidant enzymes and modulation of cellular redox status in lens cells. Arch Pharm Res 2006; 29:577-581.
8. Liu WH, Hei ZQ, Nie H, Tang FT, Huang HQ, Li XJ, et al. Berberine ameliorates renal injury in streptozotocin-induced diabetic rats by suppression of both oxidative stress and aldose reductase. Chin Med J (Engl) 2008; 121:706-712.
9. Tamadon MR, Zahmatkesh M, Beladi Mousavi SS. Administration of anti-oxidants in chronic kidney disease. J Nephropharmacolo 2015; 4:9-11.
10. Hasanvand A, Pirzadroozbahani N, Ahmadizar F, Kharazmkia A, Mir S, Baharvand P, et al. Evaluation of the anti-oxidant effects of zolpidem in the rat model of cisplatin-induced nephrotoxicity. Journal of Renal Injury Prevention 2018; 7:235-239.
11. Bhattacharya S, Manna P, Gachhui R, Sil PC. D-saccharic acid 1,4-lactone protects diabetic rat kidney by ameliorating hyperglycemia-mediated oxidative stress and renal inflammatory cytokines via NF-kappaB and PKC signaling. Toxicol Appl Pharmacol 2013; 267:16-29.
12. Lee BT, Ahmed FA, Hamm LL, Teran FJ, Chen CS, Liu Y, et al. Association of C-reactive protein, tumor necrosis factor-alpha, and interleukin-6 with chronic kidney disease. BMC Nephrol 2015; 16:77.
13. Roshan B, Stanton RC. A story of microalbuminuria and diabetic nephropathy. J Nephropathol 2013; 2:234-240.
14. Bahmani F, Bathaie SZ, Aldavood SJ, Ghahghaei A. Glycine therapy inhibits the progression of cataract in streptozotocin-induced diabetic rats. Mol Vis 2012; 18:439-348.
15. Jafarnejad A, Bathaie SZ, Nakhjavani M, Hassan MZ, Banasadegh S. The improvement effect of L-Lys as a chemical chaperone on STZ-induced diabetic rats, protein structure and function. Diabetes Metab Res Rev 2008; 24:64-73.
16. Feng RN, Niu YC, Sun XW, Li Q, Zhao C, Wang C, et al. Histidine supplementation improves insulin resistance through suppressed inflammation in obese women with the metabolic syndrome: a randomised controlled trial. Diabetologia 2013; 56:985-994.
17. Jiang WD, Qu B, Feng L, Jiang J, Kuang SY, Wu P, et al. Histidine prevents Cu-induced oxidative stress and the associated decreases in mRNA from encoding tight junction proteins in the intestine of grass carp (Ctenopharyngodon idella). PLoS One 2016; 11.
18. Abe H. Role of histidine-related compounds as intracellular proton buffering constituents in vertebrate muscle. Biochemistry (Mosc) 2000; 65:757-765.
19. Lee YT, Hsu CC, Lin MH, Liu KS, Yin MC. Histidine and carnosine delay diabetic deterioration in mice and protect human low density lipoprotein against oxidation and glycation. Eur J Pharmacol 2005; 513:145-150.
20. Watanabe M, Suliman ME, Qureshi AR, Garcia-Lopez E, Barany P, Heimburger O, et al. Consequences of low plasma histidine in chronic kidney disease patients: associations with inflammation, oxidative stress, and mortality. Am J Clin Nutr 2008; 87:1860-1866.
21. Masiello P, Broca C, Gross R, Roye M, Manteghetti M, Hillaire-Buys D, et al. Experimental NIDDM: development of a new model in adult rats administered streptozotocin and nicotinamide. Diabetes 1998; 47:224-229.
22. Satheesh MA, Pari L. Effect of pterostilbene on lipids and lipid profiles in streptozotocin-nicotinamide induced type 2 diabetes mellitus. J Appl Biomed (De Gruyter Open) 2008; 6:31–37.
23. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972; 18:499-502.
24. Ikewuchi C. Alteration of plasma lipid profiles and atherogenic indices by Stachytarpheta jamaicensis L.(Vahl). Biokemistri 2009; 21:71-77.
25. Ahmadvand H, Shahsavari G, Tavafi M, Bagheri S, Moradkhani MR, Kkorramabadi RM, et al. Protective effects of oleuropein against renal injury oxidative damage in alloxan-induced diabetic rats; a histological and biochemical study. J Nephropathol 2017; 6:204-209.
26. Tavafi M, Ahmadvand H, Khalatbari A, Tamjidipoor A. Rosmarinic acid ameliorates diabetic nephropathy in uninephrectomized diabetic rats. Iran J Basic Med Sci 2011; 14:275-283.
27. Ahmadvand H, Tavafi M. Amelioration of glomerulosclerosis by Satureja khozestanica essential oil in alloxan-induced diabetic rats. ZJRMS 2014; 16:23-26.
28. Mahdavifard S, Bathaie SZ, Nakhjavani M, Heidarzadeh H. l-cysteine is a potent inhibitor of protein glycation on both albumin and LDL, and prevents the diabetic complications in diabetic–atherosclerotic rat. Food Res Int 2014; 62:909-916.
29. Doi M, Yamaoka I, Nakayama M, Sugahara K, Yoshizawa F. Hypoglycemic effect of isoleucine involves increased muscle glucose uptake and whole body glucose oxidation and decreased hepatic gluconeogenesis. Am J Physiol Endocrinol Metab 2007; 292:E1683-1693.
30. Kimura K, Nakamura Y, Inaba Y, Matsumoto M, Kido Y, Asahara S, et al. Histidine augments the suppression of hepatic glucose production by central insulin action. Diabetes 2013; 62:2266-2277.
31. Wijekoon EP, Skinner C, Brosnan ME, Brosnan JT. Amino acid metabolism in the Zucker diabetic fatty rat: effects of insulin resistance and of type 2 diabetes. Can J Physiol Pharmacol 2004; 82:506-514.
32. Rouhi H, Ganji F. Effects of N-acetyl cysteine on serum lipoprotein (a) and proteinuria in type 2 diabetic patients. J Nephropathol 2013; 2:61-66.
33. Mong MC, Chao CY, Yin MC. Histidine and carnosine alleviated hepatic steatosis in mice consumed high saturated fat diet. Eur J Pharmacol 2011; 653:82-88.
34. Borsheim E, Bui QU, Tissier S, Cree MG, Ronsen O, Morio B, et al. Amino acid supplementation decreases plasma and liver triacylglycerols in elderly. Nutrition 2009; 25:281-288.
35. Jamor P, Ahmadvand H, Ashoory H, Babaeenezhad E. Effect of alpha-lipoic acid on anti-oxidant gene expression and kidney injury in alloxan-induced diabetic rats. J Nephropathol 2019; 8.
36. Yatzidis H. Oral supplement of six selective amino acids arrest progression renal failure in uremic patients. Int Urol Nephrol 2004; 36:591-598.
37. Sheela N, Jose MA, Sathyamurthy D, Kumar BN. Effect of silymarin on streptozotocin-nicotinamide-induced type 2 diabetic nephropathy in rats. Iran J Kidney Dis 2013; 7:117-123.
38. Faddah LM, Abdel Baky NA, Al-Rasheed NM, Al-Rasheed NM, Fatani AJ, Atteya M. Role of quercetin and arginine in ameliorating nano zinc oxide-induced nephrotoxicity in rats. BMC Complement Altern Med 2012; 12:60.
39. Sadar S, Kaspate D, Vyawahare N. Protective effect of L-glutamine against diabetes-induced nephropathy in experimental animal: Role of KIM-1, NGAL, TGF-beta1, and collagen-1. Ren Fail 2016; 38:1483-1495.
40. Arivazhagan P, Thilakavathy T, Panneerselvam C. Antioxidant lipoate and tissue anti-oxidants in aged rats. J Nutr Biochem 2000; 11:122-127.
41. Ahmadvand H, Tavafi M, Khosrowbeygi A. Amelioration of altered anti-oxidant enzymes activity and glomerulosclerosis by coenzyme Q10 in alloxan-induced diabetic rats. J Diabetes Complications 2012; 26:476-482.
42. Aboonabi A, Rahmat A, Othman F. Anti-oxidant effect of pomegranate against streptozotocin-nicotinamide generated oxidative stress induced diabetic rats. Toxicol Rep 2014; 1:915-922.
43. Yan SL, Wu ST, Yin MC, Chen HT, Chen HC. Protective effects from carnosine and histidine on acetaminophen-induced liver injury. J Food Sci 2009; 74:259-265.
44. Watanabe M, Nakashima H, Mochizuki S, Abe Y, Ishimura A, Ito K, et al. Amelioration of diabetic nephropathy in OLETF rats by prostaglandin I(2) analog, beraprost sodium. Am J Nephrol 2009; 30:1-11.
45. Cheng H, Harris RC. Renal endothelial dysfunction in diabetic nephropathy. Cardiovasc Hematol Disord Drug Targets 2014; 14:22-33.
46. Gorudko I, Kostevich A, Sokolov A, Konstatinova E, Tsapaeva N, Mironova E, et al. Increased myelopepoxidase activity is a risk factor for ishemic heart disease in patients with diabetes mellitus. Biomeditsinskaia khimiia 2012; 58:475-484.
47. Vita JA, Brennan ML, Gokce N, Mann SA, Goormastic M, Shishehbor MH, et al. Serum myeloperoxidase levels independently predict endothelial dysfunction in humans. Circulation 2004; 110:1134-1139.
48. Madar Z, Kalet-Litman S, Stark AH. Inducible nitric oxide synthase activity and expression in liver and hepatocytes of diabetic rats. Pharmacology 2005; 73:106-112.
49. Zhang H, Tsao RJCOiFS. Dietary polyphenols, oxidative stress and anti-oxidant and anti-inflammatory effects.  2016; 8:33-42.
50. Yagmurca M, Erdogan H, Iraz M, Songur A, Ucar M, Fadillioglu E. Caffeic acid phenethyl ester as a protective agent against doxorubicin nephrotoxicity in rats. Clin Chim Acta 2004; 348:27-34.
51. Todorova VK, Kaufmann Y, Hennings L, Klimberg VS. Oral glutamine protects against acute doxorubicin-induced cardiotoxicity of tumor-bearing rats. J Nutr 2010; 140:44-48.
52. Navarro JF, Milena FJ, Mora C, Leon C, Garcia J. Renal pro-inflammatory cytokine gene expression in diabetic nephropathy: effect of angiotensin-converting enzyme inhibition and pentoxifylline administration. Am J Nephrol 2006; 26:562-570.
53. Andou A, Hisamatsu T, Okamoto S, Chinen H, Kamada N, Kobayashi T, et al. Dietary histidine ameliorates murine colitis by inhibition of proinflammatory cytokine production from macrophages. Gastroenterology 2009; 136:564-574.e562.
54. Sadi G, Eryilmaz N, Tutuncuoglu E, Cingir S, Guray T. Changes in expression profiles of anti-oxidant enzymes in diabetic rat kidneys. Diabetes Metab Res Rev 2012; 28:228-235.
55. Matsunami T, Sato Y, Sato T, Ariga S, Shimomura T, Yukawa M. Oxidative stress and gene expression of anti-oxidant enzymes in the streptozotocin-induced diabetic rats under hyperbaric oxygen exposure. Int J Clin Exp Pathol 2010; 3:177-188.
56. Cao C, Leng Y, Huang W, Liu X, Kufe D. Glutathione peroxidase 1 is regulated by the c-Abl and Arg tyrosine kinases. J Biol Chem 2003; 278:39609-39614.
57. Reddi AS, Bollineni JS. Renal cortical expression of mRNAs for anti-oxidant enzymes in normal and diabetic rats. Biochem Biophys Res Commun 1997; 235:598-601.
58. Limaye PV, Raghuram N, Sivakami S. Oxidative stress and gene expression of anti-oxidant enzymes in the renal cortex of streptozotocin-induced diabetic rats. Mol Cell Biochem 2003; 243:147-152.