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2023, Vol: 13, Issue: 5
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Original Research 


Effect of combining an angiotensin-converting enzyme inhibitor and a vitamin D receptor activator on renal oxidative and nitrosative stress in diabetic rats

Tarek Mohamed Ali, Basem Hassan El Esawy, Elsayed A Elmorsy.

Cited By: 6

Abstract
Background: Diabetic nephropathy (DN) is a progressive and irreversible renal disease. Experimental researches have established the role of oxidative stress as a central factor in pathogenesis, onset, and advancement of DN.

Aims and Objectives: To investigate the effect of the combined treatment with angiotensin-converting enzyme inhibitor, enalapril, and the specific vitamin D receptor activator paricalcitol, alone or in combination, using a diabetic rat model.

Materials and Methods: Fifty rats were divided into five groups of 10 rats each. Diabetes was induced by a single intraperitoneal injection of streptozotocin (50 mg/kg bw). Group 1 consisting of normal rats was served as control group. Group 2 was treated with vehicle (100 μl propylene glycol ip), group 3 was treated with enalapril (25 mg/l in drinking water), group 4 was treated with paricalcitol (0.8 μg/kg ip, 3 × weeks), and group 5 was treated with both drugs. The rats were treated for 3 months. Biochemical analysis was performed using an automatic biochemistry analyzer. Evaluation of oxidant/antioxidant balance and immunohistochemical localization of 3-nitrotyrosine (3-NT) in the kidney tissue was performed.

Results: Combined treatment with both drugs was associated with significantly lower blood glucose, malondialdehyde, nitric oxide, levels and significantly higher levels of the antioxidant parameters more than those observed for monotherapy. Co-treatment led to additional improvement with negligible interstitial damage with no glomerular or tubular injury detected and strongly decreased 3-NT expression induced by diabetes.

Conclusion: Co-treatment with both drugs exerts a synergistic protective effect against diabetic nephropathy by decreasing oxidative and nitrosative stress.

Key words: Enalapril; Paricalcitol; Oxidative and Nitrosative Stress; Diabetic Nephropathy; Rats


 
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REFERENCES
1. International Diabetes Federation. IDF Diabetes Atlas, 6th edn. Brussels, Belgium: International Diabetes Federation, 2013.
2. Dunn WB, Broadhurst DI, Atherton HJ, Goodacre R, Griffin JL. Systems level studies of mammalian metabolomes: the roles of mass spectrometry and nuclear magnetic resonance spectroscopy. Chem Soc Rev. 2011;40:387-426. [DOI via Crossref]    [Pubmed]   
3. Vasavada N, Agarwal R. Role of oxidative stress in diabetic nephropathy. Adv Chronic Kidney Dis. 2005;12:146-54. [DOI via Crossref]    [Pubmed]   
4. Kang ES, Lee GT, Kim BS, Kim CH, Seo GH, Han SJ, et al. Lithospermic acid B ameliorates the development of diabetic nephropathy in OLETF rats. Eur J Pharmacol. 2008;579:418-25. [DOI via Crossref]    [Pubmed]   
5. Groop PH, Thomas MC, Moran JL, Wadèn J, Thorn LM, Mäkinen VP, et al. Finn Diane Study Group. The presence and severity of chronic kidney disease predicts all-cause mortality in type 1 diabetes. Diabetes. 2009;7:1651-8. [DOI via Crossref]    [Pubmed]    [PMC Free Fulltext]   
6. Mshelia DS. Role of free radicals in pathogenesis of diabetic nephropathy: Ann Afr Med. 2004;3:55-62.
7. Sayed AA, Khalifa M, Abd el-Latif FF. Fenugreek attenuation of diabetic nephropathy in alloxan-diabetic rats: attenuation of diabetic nephropathy in rats. J Physiol Biochem. 2012;68:263-9. [DOI via Crossref]    [Pubmed]   
8. Tavafi M. Diabetic nephropathy and antioxidants: J Nephropathol. 2013;2:20-7. [DOI via Crossref]    [Pubmed]    [PMC Free Fulltext]   
9. Ha H, Hwang IA, Park JH, Lee HB. Role of reactive oxygen species in the pathogenesis of diabetic nephropathy. Diabetes Res Clin Pract. 2008;82:s42-5. [DOI via Crossref]    [Pubmed]   
10. Choi SW, Benzie IF, Ma SW, Strain JJ, Hannigan BM. Acute hyperglycemia and oxidative stress: direct cause and effect? Free Radic Biol Med. 2008;44:1217-31. [DOI via Crossref]    [Pubmed]   
11. Jacobson HR. Chronic renal failure: pathophysiology. Lancet. 1991;338:419-23. [DOI via Crossref]   
12. 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;142:317-27. [DOI via Crossref]    [Pubmed]   
13. Stephens JW, Khanolkar MP, Bain SC. The biological relevance and measurement of plasma markers of oxidative stress in diabetes and cardiovascular disease. Atherosclerosis. 2009;202:321-9. [DOI via Crossref]    [Pubmed]   
14. Onozato ML, Tojo A, Goto A, Fujita T, Wilcox CS. Oxidative stress and nitric oxide synthase in rat diabetic nephropathy: effects of ACEI and ARB. Kidney Int. 2002;61:186-94. [DOI via Crossref]    [Pubmed]   
15. Beisswenger PJ, Howell SK, Russell GB, Miller ME, Rich SS, Mauer M. Early progression of diabetic nephropathy correlates with methylglyoxal-derived advanced glycation end products. Diabetes Care. 2013;36:3234-9. [DOI via Crossref]    [Pubmed]    [PMC Free Fulltext]   
16. Noiri E, Nakao A, Uchida K, Tsukahara H, Ohno M, Fujita T, et al. Oxidative and nitrosative stress in acute renal ischemia. Am J Physiol Renal Physiol. 2001;281:F948-F957. [DOI via Crossref]    [Pubmed]   
17. Ishii N, Ikenaga H, Carmines PK, Takada N, Okazaki T, Nagai T, et al. Impact of angiotensin-converting enzyme inhibition on renal cortical nitrotyrosine content during increased extracellular glucose concentration. Clin Biochem. 2006;39:633-9. [DOI via Crossref]    [Pubmed]   
18. Valdivielso JM. The physiology of vitamin D receptor activation. Contrib Nephrol. 2009;163:206-12. [DOI via Crossref]    [Pubmed]   
19. Schwarz U, Amann K, Orth SR, Simonaviciene A, Wessels S, Ritz E. Effect of 1,25(OH)2 vitamin D-3 on glomerulosclerosis in subtotally nephrectomized rats. Kidney Int. 1998;53:1696-705. [DOI via Crossref]    [Pubmed]   
20. Zhang Z, Zhang Y, Ning G, Deb DK, Kong J, Li YC. Combination therapy with AT1 blocker and vitamin D analog markedly ameliorates diabetic nephropathy: blockade of compensatory renin increase. Proc Natl Acad Sci USA. 2008;105:15896-901. [DOI via Crossref]    [Pubmed]    [PMC Free Fulltext]   
21. Agarwal R, Acharya M, Tian J, Hippensteel RL, Melnick JZ, Qiu P, et al. Antiproteinuric effect of oral paricalcitol in chronic kidney disease. Kidney Int. 2005;68:2823-8. [DOI via Crossref]    [Pubmed]   
22. Mizobuchi M, Morrissey J, Finch JL, Martin DR, Liapis H, Akizawa T, et al. Combination therapy with an angiotensin-converting enzyme inhibitor and a vitamin D analog suppresses the progression of renal insufficiency in uremic rats. J Am Soc Nephrol. 2007;18: 1796-1806. [DOI via Crossref]    [Pubmed]   
23. Husain K, Suarez E, Isidro A, Ferder L. Effects of paricalcitol and enalapril on atherosclerotic injury in mouse aortas: Am J Nephrol. 2010;32:296-304. [DOI via Crossref]    [Pubmed]   
24. Finch JL, Suarez EB, Husain K, Ferder L, Cardema MC, Glenn DJ, et al. Effect of combining an ACE inhibitor and a VDR activator on glomerulosclerosis, proteinuria, and renal oxidative stress in uremic rats. Am J Physiol Renal Physiol. 2012;302:F141-9. [DOI via Crossref]    [Pubmed]   
25. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem. 1976;72:248-54. 26. Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121-6. [DOI via Crossref]   
27. Lawrence RA, Burk RF. Glutathione peroxidase activity in selenium deficient rat liver. Biochem Biophys Res Commun. 1976;71:952-8. [DOI via Crossref]   
28. Sun Y, Oberley LW, Li Y. A simple method for clinical assay of superoxide dismutase. Clin Chem. 1988;34:497-500. [Pubmed]   
29. Draper H, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 1990;186:421-31. [DOI via Crossref]   
30. Placer ZA, Cushman LL, Johnson BC. Estimation of product of lipid peroxidation (malonyldialdehyde) in biochemical systems. Anal Biochem. 1966;16:359. [DOI via Crossref]   
31. Hortelano S, Dewez B, Genaro AM, az-Guerra MJ, Bosca L. Nitric oxide is released in regenerating liver after partial hepatectomy. Hepatology. 1995;21:776-86. [Pubmed]   
32. Mizobuchi M, Morrissey J, Finch JL, Martin DR, Liapis H, Akizawa T, et al. Combination therapy with an angiotensin-converting enzyme inhibitor and a vitamin D analog suppresses the progression of renal insufficiency in uremic rats. J Am Soc Nephrol. 2007;18:1796-1806. [DOI via Crossref]    [Pubmed]   
33. Yuan W, Pan W, Kong J, Zheng W, Szeto FL, Wong KE, et al. 1,25-Dihydroxyvitamin D3 suppresses renin gene transcription by blocking the activity of the cyclic AMP response element in the renin gene promoter. J Biol Chem. 2007;282:29821-30. [DOI via Crossref]    [Pubmed]   
34. Lewis EJ, Hunsicker LG, Bain RP, Rohde RD. The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. The Collaborative Study Group. N Engl J Med. 1993;329:1456-62. [DOI via Crossref]    [Pubmed]   
35. Zafari AM, Ushio-Fukai M, Akers M, Yin Q, Shah A, Harrison DG, et al. Role of NADH/NADPH oxidase-derived H2O2 in angiotensin II-induced vascular hypertrophy. Hypertension. 1998;32:488-95. [DOI via Crossref]    [Pubmed]   
36. Baynes JW, Thorpe SR. The role of oxidative stress in diabetic complications. Curr Opin Endocrinol. 1996;3:277-84. [DOI via Crossref]   
37. Turk HM, Sevinc A, Camci C, Cigli A, Buyukberber S, Savli H, et al. Plasma lipid peroxidation products and antioxidant enzyme activities in patients with type 2 diabetes mellitus. Acta Diabetologica. 2002;39:117-22. [DOI via Crossref]    [Pubmed]   
38. Kim H, Kang K, Yamabe N, Yokozawa T. Comparison of the effects of Korean ginseng and heat-processed Korean ginseng on diabetic oxidative stress. Am J Chin Med. 2008;36:989-1004. [DOI via Crossref]    [Pubmed]   
39. Kakkar R, Mantha SV, Radhi J, Prasad K, Kalra J. Antioxidant defense system in diabetic kidney: a time course study. Life Sci. 1997;60:667-79. [DOI via Crossref]   
40. De Souza Santos R, Vianna LM. Effects of cholecalciferol supplementation on blood glucose in an experimental model of type 2 diabetes mellitus in spontaneously hypertensive rats and Wistar rats. Clin Chim Acta. 2005;358:146-50. [DOI via Crossref]    [Pubmed]   
41. Baynes KC, Boucher BJ, Feskens EJ, Kromhout D. Vitamin D, glucose tolerance and insulinaemia in elderly men. Diabetologia. 1997; 40:344-7. [DOI via Crossref]    [Pubmed]   
42. Maestro B, Campion J, Davila N, Calle C. Stimulation by 1, 25-dihydroxyvitamin D3 of insulin receptor expression and insulin responsiveness for glucose transport in U-937 human promonocytic cells. Endocr J. 2000;47:383-91. [DOI via Crossref]    [Pubmed]   
43. Borissova AM, Tankova T, Kirilov G, Dakovska L, Kovacheva R. The effect of vitamin D3 on insulin secretion and peripheral insulin sensitivity in type 2 diabetic patients. Int J Clin Pract. 2003;57:258-61. [Pubmed]   
44. Chiu KC, Chuang LM, Lee NP, Ryu JM, McGullam JL, Tsai GP, et al. Insulin sensitivity is inversely correlated with plasma intact parathyroid hormone level. Metabolism. 2000;49:1501-05. [DOI via Crossref]    [Pubmed]   
45. Gaweł S, Wardas M, Niedworok E, Wardas P. Malondialdehyde (MDA) as a lipid peroxidation marker. WiadLek. 2004;57:453-5.
46. Michel T, Feron O. Nitric oxide syntheses: which, where, how, and why? J Clin Invest. 1997;100:2146-52. [DOI via Crossref]    [Pubmed]    [PMC Free Fulltext]   
47. Vaziri ND, Ni Z, Oveisi F, Trnavsky-Hobbs DL. Effect of antioxidant therapy on blood pressure and NO synthase expression in hypertensive rats. Hypertension. 2000;36:957-64. [DOI via Crossref]    [Pubmed]   
48. Somani SM, Husain K, Schlorff E. Response of antioxidant system to physical and chemical stress. In: Baskin SI, Salem H (Eds.), Oxidants, Antioxidants and Free Radicals. Washington, DC: Taylor and Francis, 1997, pp. 125-141.
49. Marcondes S, Cardoso MH, Morganti RP, Thomazzi SM, Lilla S, Murad F. Cyclic GMP-independent mechanisms contribute to the inhibition of platelet adhesion by nitric oxide donor: a role for {alpha}-actinin nitration. Proc Natl Acad Sci. 2006;103: 3434-9. [DOI via Crossref]    [Pubmed]    [PMC Free Fulltext]   
50. Marklund SL. Regulation of cytokines of extracellular superoxide dismutase and other superoxide dismutase isozymes in fibroblasts. J Biol Chem. 1992;267:6696-701. [Pubmed]   
51. Godin DV, Wohaieh SA, Garnett ME, Goumeniouk AD. Antioxidant enzyme alterations in experimental and clinical diabetes. Mol Cell Biochem. 1988;84:223-31. [DOI via Crossref]    [Pubmed]   
52. Limaye PV, Raghuram N, Sivakami S. Oxidative stress and gene expression of antioxidant enzymes in the renal cortex of streptozotocin induced diabetic rats. Mol Cell Biochem. 2003;243: 147-52. [DOI via Crossref]    [Pubmed]   
53. Ishii N, Patel KP, Lane PH, Taylor T, Bian K, Murad F, et al. Nitric oxide synthesis and oxidative stress in the renal cortex of rats with diabetes mellitus. J Am Soc Nephrol. 2001;12:1630-9. [Pubmed]   
54. Hayes JD, Flanagan JU, Jowsey IR. Glutathione transferases. Annu Rev Pharmacol Toxicol. 2005;45:51-88. [DOI via Crossref]    [Pubmed]   
55. Thuraisingham RC, Nott CA, Dodd SM, Yaqoob MM. Increased nitrotyrosine staining in kidneys from patients with diabetic nephropathy. Kidney Int. 2000;57:1968-72. [DOI via Crossref]    [Pubmed]   
56. Pacher P, Obrosova I, Mabley J, Szabó C. Role of nitrosative stress and peroxynitrite in the pathogenesis of diabetic complications: emerging new therapeutical strategies. Curr Med Chem. 2005;12:267-75. [DOI via Crossref]    [Pubmed]    [PMC Free Fulltext]   
57. Beckman JS, Koppenol WH. Nitric oxide, superoxide and peroxynitrite, the good, the bad and the ugly. Am J Physiol. 1996;271: C1424-C1437. [Pubmed]   
58. DeRubertis FR, Craven PA, Melhem MF, Salah EM. Attenuation of renal injury in db/db mice overexpressing superoxide dismutase: evidence for reduced superoxide-nitric oxide interaction. Diabetes. 2004;53:762-68. [DOI via Crossref]    [Pubmed]   
59. Emam MA. Comparative evaluation of antidiabetic activity of Rosmarinus officinalis L. and Chamomile recutita in streptozotocin induced diabetic rats. Agric Biol J N Am. 2012;3:247-52 [DOI via Crossref]   

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How to Cite this Article
Pubmed Style

Tarek Mohamed Ali, Basem Hassan El Esawy, Elsayed A Elmorsy. Effect of combining an angiotensin-converting enzyme inhibitor and a vitamin D receptor activator on renal oxidative and nitrosative stress in diabetic rats. Natl J Physiol Pharm Pharmacol. 2015; 5(3): 222-231. doi:10.5455/njppp.2015.5.1401201522

Web Style

Tarek Mohamed Ali, Basem Hassan El Esawy, Elsayed A Elmorsy. Effect of combining an angiotensin-converting enzyme inhibitor and a vitamin D receptor activator on renal oxidative and nitrosative stress in diabetic rats. https://www.njppp.com/?mno=177563 [Access: May 01, 2023]. doi:10.5455/njppp.2015.5.1401201522

AMA (American Medical Association) Style

Tarek Mohamed Ali, Basem Hassan El Esawy, Elsayed A Elmorsy. Effect of combining an angiotensin-converting enzyme inhibitor and a vitamin D receptor activator on renal oxidative and nitrosative stress in diabetic rats. Natl J Physiol Pharm Pharmacol. 2015; 5(3): 222-231. doi:10.5455/njppp.2015.5.1401201522


Vancouver/ICMJE Style

Tarek Mohamed Ali, Basem Hassan El Esawy, Elsayed A Elmorsy. Effect of combining an angiotensin-converting enzyme inhibitor and a vitamin D receptor activator on renal oxidative and nitrosative stress in diabetic rats. Natl J Physiol Pharm Pharmacol. (2015), [cited May 01, 2023]; 5(3): 222-231. doi:10.5455/njppp.2015.5.1401201522


Harvard Style

Tarek Mohamed Ali, Basem Hassan El Esawy, Elsayed A Elmorsy (2015) Effect of combining an angiotensin-converting enzyme inhibitor and a vitamin D receptor activator on renal oxidative and nitrosative stress in diabetic rats. Natl J Physiol Pharm Pharmacol, 5 (3), 222-231. doi:10.5455/njppp.2015.5.1401201522


Turabian Style

Tarek Mohamed Ali, Basem Hassan El Esawy, Elsayed A Elmorsy. 2015. Effect of combining an angiotensin-converting enzyme inhibitor and a vitamin D receptor activator on renal oxidative and nitrosative stress in diabetic rats. National Journal of Physiology, Pharmacy and Pharmacology, 5 (3), 222-231. doi:10.5455/njppp.2015.5.1401201522


Chicago Style

Tarek Mohamed Ali, Basem Hassan El Esawy, Elsayed A Elmorsy. "Effect of combining an angiotensin-converting enzyme inhibitor and a vitamin D receptor activator on renal oxidative and nitrosative stress in diabetic rats." National Journal of Physiology, Pharmacy and Pharmacology 5 (2015), 222-231. doi:10.5455/njppp.2015.5.1401201522


MLA (The Modern Language Association) Style

Tarek Mohamed Ali, Basem Hassan El Esawy, Elsayed A Elmorsy. "Effect of combining an angiotensin-converting enzyme inhibitor and a vitamin D receptor activator on renal oxidative and nitrosative stress in diabetic rats." National Journal of Physiology, Pharmacy and Pharmacology 5.3 (2015), 222-231. Print. doi:10.5455/njppp.2015.5.1401201522


APA (American Psychological Association) Style

Tarek Mohamed Ali, Basem Hassan El Esawy, Elsayed A Elmorsy (2015) Effect of combining an angiotensin-converting enzyme inhibitor and a vitamin D receptor activator on renal oxidative and nitrosative stress in diabetic rats. National Journal of Physiology, Pharmacy and Pharmacology, 5 (3), 222-231. doi:10.5455/njppp.2015.5.1401201522


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