Effects of enalapril and paricalcitol treatment on diabetic nephropathy and renal expressions of TNF-α, p53, caspase-3 and Bcl-2 in STZ-induced diabetic rats
Autoři:
Osama M. Ahmed aff001; Tarek M. Ali aff002; Mohamed A. Abdel Gaid aff001; Ahmed A. Elberry aff004
Působiště autorů:
Experimental Obesity and Diabetes Research Lab, Physiology Division, Zoology Department, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt
aff001; Department of Clinical Laboratories, College of Applied Medical Sciences, Taif University, Taif, Saudi Arabia
aff002; Department of Physiology, Faculty of Medicine, Beni-Suef University, Beni-Suef, Egypt
aff003; Clinical Pharmacology Department, Faculty of Medicine, Beni-Suef University, Beni-suef, Egypt
aff004
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0214349
Souhrn
This study aimed to assess the renopreventive effect of enalapril and/or paricalcitol on streptozotocin (STZ) diabetes-induced nephropathy and to elucidate their mechanisms of action through investigation of the effects on renal oxidative stress, antioxidant defense system and expressions of TNF-α, p53, caspase-3, and Bcl-2. Diabetes mellitus was induced in fasting male Wistar rats by single intraperitoneal injection of STZ (45 mg /kg b.w.) dissolved in citrate buffer (pH 4.5). Ten days after STZ injection, the diabetic rats were treated with enalapril (25 mg/l of drinking water) and/or paricalcitol (8 μg/kg b.w. per os) dissolved in 5% DMSO daily for 4 weeks. The obtained data revealed that the treatment of diabetic Wistar rats with enalapril and/or paricalcitol led to significant decreases in the elevated serum urea, uric acid, creatinine, sodium and potassium levels; thereby reflecting the improvement of the impaired kidney function. The deteriorated kidney lipid peroxidation, GSH content and GST and catalase activities in diabetic rats were significantly ameliorated as a result of treatment with enalapril and/or paricalcitol. The elevated fasting and post-prandial serum glucose levels and the lowered serum insulin and C-peptide levels were also improved. The treatment with enalapril and paricalcitol in combination was the most potent in decreasing the elevated serum glucose levels. Moreover, the treatment of diabetic rats successfully prevented the diabetes-induced histopathological deleterious changes of kidney and islets of Langerhans of pancreas. In association, the immunohistochemically detected pro-inflammatory cytokine, TNF-α, and apoptotic mediators, p53 and caspase-3, were remarkably decreased in kidney of diabetic rats as a result of treatment while the expression of anti-apoptotic protein Bcl-2 was increased. Based on these findings, it can be concluded that enalapril and paricalcitol alone or in combination can prevent STZ diabetes-induced nephropathy through amelioration of the glycemic state and antioxidant defense system together with the suppression of oxidative stress, inflammation and apoptosis. However, the treatment of diabetic rats with enalapril and paricalcitol in combination has no further significant improvement effects on renal function and damage when compared with enalapril or paclitaxel treated diabetic groups.
Klíčová slova:
Biology and life sciences – Cell biology – Biochemistry – Cell processes – Developmental biology – Anatomy – Medicine and health sciences – Physiology – Endocrinology – Endocrine disorders – Metabolic disorders – Immunology – Immune system – Innate immune system – Cytokines – Diabetic endocrinology – Insulin – Immune physiology – Hormones – Molecular development – Cell death – Apoptosis – Renal system – Kidneys – Antioxidants – Oxidative stress
Zdroje
1. Lim AK. Diabetic nephropathy–complications and treatment. Int J Nephrol Renovasc Dis. 2014; 7: 361–381. doi: 10.2147/IJNRD.S40172 25342915
2. Piscitelli P, Viazzi F, Fioretto P, Giorda C, Ceriello A, Genovese S, et al. Predictors of chronic kidney disease in type 1 diabetes: a longitudinal study from the AMD Annals initiative. Sci Re. 2017; 7: 3313.
3. Gheith O, Farouk N, Nampoory N, Halim MA, Al-Otaibi T. Diabetic kidney disease: worldwide difference of prevalence and risk factors. J Nephropharmacol. 2016; 5(1): 49–56. 28197499
4. International Diabetes Federation. Diabetes Atlas 7th Edition International Diabetes Federation. http://www.idf.org/idf-diabetes-atlas-seventh-edition, 2016.
5. Patschan D, Müller GA. Acute Kidney Injury in Diabetes Mellitus. Int J Nephrol. 2016; Article ID 6232909, 7 pages.
6. Hoshino J, Mise K, Ueno T, Imafuku A, Kawada M, Sumida K, et al. A pathological scoring system to predict renal outcome in diabetic nephropathy. Am J Nephrol 2015; 41: 337–344. doi: 10.1159/000431333 26067713
7. Anderson S, Komers R. Inhibition of the renin-angiotensin system: is more better? Kidney Int. 2009; 75: 12–14. doi: 10.1038/ki.2008.556 19092813
8. Lewis EJ, Hunsicker LG, Bain RP, Rohde RD. The effect of angiotensin-converting–enzyme inhibition on diabetic nephropathy. N Engl J Med. 1993; 329: 1456–1462. [Erratum, N Engl J Med 1993; 330: 152].
9. Capes SE, Gerstein HC, Negassa A, Yusuf S. Enalapril prevents clinical proteinuria in diabetic patients with low ejection fraction. Diabetes Care 2000; 23(3): 377–80. doi: 10.2337/diacare.23.3.377 10868869
10. Tylicki L, Lizakowski B. Renin-angiotensin-aldosterone system blockade for nephroprotection: current evidence and future directions. J Nephrol. 2012; 25: 900–910. doi: 10.5301/jn.5000134 22684647
11. Vermes E, Ducharme A, Bourassa MG, Lessard M, White M, Tardif J. Enalapril reduces the incidence of diabetes in patients with chronic heart failure: insight from the studies of left ventricular dysfunction (SOLVD). Circulation. 2003; 107: 1291–1296. doi: 10.1161/01.cir.0000054611.89228.92 12628950
12. Shamiss A, Carroll J, Peleg E, Grossman E, Rosenthal T. The effect of enalapril with and without hydrochlorothiazide on insulin sensitivity and other metabolic abnormalities of hypertensive patients with NIDDM. Am J Hyperten. 8(3); 1995: 276–281.
13. Freundlich M, Quiroz Y, Zhang Z, Zhang Y, Bravo Y, Weisinger JR, et al. Suppression of renin-angiotensin gene expression in the kidney by paricalcitol. Kidney Int 2008; 74: 1394–402. doi: 10.1038/ki.2008.408 18813285
14. Rammos G, Tseke P, Ziakka S. Vitamin D, the renin-angiotensin system, and insulin resistance. Int Urol Nephrol. 2008; 40: 419–426 doi: 10.1007/s11255-007-9244-4 18193490
15. Mizobuchi M, Morrisey 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: 10.1681/ASN.2006091028 17513326
16. Aperis G, Paliouras C, Zervos A, Arvanitis A, Alivanis P. The role of paricalcitol on proteinuria. J Ren Care 2011; 37(2): 80–84. doi: 10.1111/j.1755-6686.2011.00229.x 21561543
17. Izquierdo MJ, Cavia M, Muniz P, De Francisco AL, Arias M, Santos J et al. Paricalcitol reduced oxidative stress and inflammation in hemodialysis patients. BMC Nephrol 2012; 13: 159. doi: 10.1186/1471-2369-13-159 23186077
18. Li YC, Kong J, Wei M, Chen ZF, Liu SQ, Cao LP. 1,25-Dihydroxyvitamin D(3) is a negative endocrine regulator of the renin-angiotensin system. J Clin Invest. 2002; 110: 229–238. doi: 10.1172/JCI15219 12122115
19. 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–F149. doi: 10.1152/ajprenal.00293.2011 21957179
20. Ali TM, Mehanna OM, Elsaid AG, ElAskary A. Effect of Combination of Angiotensin-Converting Enzyme Inhibitors and Vitamin D Receptor Activatorson Cardiac Oxidative Stress in Diabetic Rats. Am J Med Sci. 2016; 352(2): 208–214. doi: 10.1016/j.amjms.2016.04.016 27524220
21. Husain K., Suarez E, Isidro A, Hernandez W, Ferder L. Effect of paricalcitol and enalapril on renal inflammation/oxidative stress in atherosclerosis. World J Biol Chem. 2015; 6(3): 240–248. doi: 10.4331/wjbc.v6.i3.240 26322179
22. Sagar P, J Zhang J, Mannix C, Wong A, Rangan G. Combined paricalcitol and enalapril improves hypertension but not kidney cyst growth in experimental polycystic kidney disease. Experimental Tubolointerstitial Disease, Mini Oral. http://www.anzsnasm.com/4293
23. Ahmed OM, Abdel Gabar M, Ali TM. Impacts of the coexistence of diabetes and hypothyroidism on body weight gain, leptin and various metabolic aspects in albino rats. J Diabetes Complications, 2012; 26: 491–500. doi: 10.1016/j.jdiacomp.2012.05.021 22770939
24. Ashour MB, Ahmed OM, Asran AA, Ali MA. Assessment of the preventive effects of Salvia officinalis and Ruta graveolens ethanolic leaf extracts on chlorpyrifos- and methomyl-induced renal toxicity and oxidative stress in albino rats. International Journal of Prevention and Treatment, 2017; 6(2): 34–44.
25. Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med. 1963; 61: 882–8. 13967893
26. Preuss HG, Jarrel ST, Scheckenobach R, Liberman S, Anderson RA. Comparative effects of chromium, vanadium and Gymnema sylvestre on sugar-induced blood pressure elevations in SHR. J Am Coll Nut. 1998; 17(2): 116–23.
27. Mannervik B, Gutenberg C. Glutathione transferase (Human placenta), Meth. Enzymol. 1981; 77: 231–5.
28. Cohen G, Dembiec D, Marcus J. Measurement of catalase activity in tissue extracts. Anal Biochem.1970; 34: 30–38. doi: 10.1016/0003-2697(70)90083-7 5440916
29. Banchroft JD, Stevens A, Turner DR. Theory and Practice of Histological Techniques. 4th Edition. Churchill Livingston, New York, London, San Francisco, Tokyo, 1996.
30. Hussein AM, Ahmed OM. Regioselective one-pot synthesis and anti-proliferative and apoptotic effects of some novel tetrazolo[1,5-a] pyrimidine derivatives. Bioorg Med Chem. 2010; 18: 2639–2644. doi: 10.1016/j.bmc.2010.02.028 20227281
31. Roa M, Blane K, Zonneberg M. PC-STAT: One-way analysis of variance," Version IA (C) copyright. University of Georgia, USA, 1985.
32. Bidani AK, Picken M, Hacioglu R, Williamson G, Griffin KA. Spontaneously reduced BP load in the rat streptozotocin-induced diabetes model: Potential pathogenetic relevance. Am J Physiol Renal Physiol. 2007; 292(2): F647–F654. doi: 10.1152/ajprenal.00017.2006 16968892
33. Zafar M, Naqvi SN. Effects of STZ-induced diabetes on the relative weights of kidney, liver and pancreas in albino rats: a comparative study. Int J Morphol. 2010; 28: 135–142.
34. Ahmed OM. Histopathological and biochemical evaluation of liver and kidney lesions in streptozotocin diabetic rats treated with glimepiride and various plant extracts," J Union Arab Biol. 2001; 16A: 585–625.
35. de Brito Amaral LS, Souza CS, Volpini RA, Shimizu MHM, de Bragança AC, Canale D, et al. Previous Exercise Training Reduces Markers of Renal Oxidative Stress and Inflammation in Streptozotocin-Induced Diabetic Female Rats. J Diab Res. 2018, Article ID 6170352, 9 pages.
36. Ziamajidi N, Nasiri A, Abbasalipourkabir R, Moheb SS. Effects of garlic extract on TNF-α expression and oxidative stress status in the kidneys of rats with STZ + nicotinamide-induced diabetes. Pharmaceut Biol. 2017; 55(1): 526–531.
37. Poljsak B, Šuput D, Milisav I. Achieving the balance between ROS and antioxidants: When to use the synthetic antioxidants. Oxid Med Cell Longev. 2013; Article ID 956792, 11 pages.
38. Nita M, Grzybowski A. The role of the reactive oxygen species and oxidative stress in the pathomechanism of the age-related ocular diseases and other pathologies of the anterior and posterior eye segments in adults. Oxid Med Cell Longev. 2016; Article ID 3164734, 23 pages.
39. Pradeep SR, Srinivasan K. Alleviation of oxidative stress-mediated nephropathy by dietary fenugreek (Trigonella foenum-graecum) seeds and onion (Allium cepa) in streptozotocin-induced diabetic rats. Food Funct. 2018; 9:134–148. doi: 10.1039/c7fo01044c 29068452
40. Sha J., Sui B., Su X., Meng Q., Zhang C. Alteration of oxidative stress and inflammatory cytokines induces apoptosis in diabetic nephropathy. Mol Med Rep. 2017; 16(5): 7715–7723. doi: 10.3892/mmr.2017.7522 28944839
41. Suarez-Martinez E, Husain K, Ferder L. Adiponectin expression and the cardioprotective role of the vitamin D receptor activator paricalcitol and the angiotensin converting enzyme inhibitor enalapril in ApoE-deficient mice. Ther Adv Cardiovasc Dis. 2014; 8(6): 224–236. doi: 10.1177/1753944714542593 25037058
42. Agrawal NK, Gupta U, Singh SP. Effects of enalapril on blood glucose level and interaction with the oral anti-diabetic drugs in alloxan-induced diabetic rats. Asian J Pharm Clin Res. 2013; 6(2): 66–69.
43. Stump CS, Hamilton MT, Sowers JR. Effect of antihypertensive agents on the development of type 2 diabetes mellitus. Mayo Clinic Proceed. 2006; 81(6): 796–806.
44. Tikellis C, Wookey PJ, Candido R, Andrikopoulos S, Thomas MC, Cooper ME. Improved islet morphology after blockade of the renin- angiotensin system in the ZDF rat. Diabetes 2004; 53: 989–997. doi: 10.2337/diabetes.53.4.989 15047614
45. Lau T, Carlsson PO, Leung PS. Evidence for a local angiotensin-generating system and dose-dependent inhibition of glucose-stimulated insulin release by angiotensin II in isolated pancreatic islets. Diabetologia 2004; 47: 240–248. doi: 10.1007/s00125-003-1295-1 14722647
46. Brown AJ, Dusso A, Slatopolsky E. Vitamin D. Am J Physiol. 1999; 277 (Renal Physiol. 46): F157–F175.
47. Gravellone L, Rizzo MA, Martina V, Mezzina N, Regalia A, Maurizio Gallieni M. Vitamin D receptor activators and clinical outcomes in chronic kidney disease. Int J Nephrol. 2011; 2011: Article ID 419524, 13 pages.
48. Christakos S, Friedlander EJ, Frandsen BR, Norman AW. Studies on the mode of action of calciferol. XIII. Development of a radioimmunoassay for vitamin D-dependent chick intestinal calcium-binding protein and tissue distribution. Endocrinol. 1979; 104: 1495–1503.
49. Rabinovitch A, Suarez-Pinzon WL, Sooy K, Strynadka K, Christakos S. Expression of calbindin-D(28k) in a pancreatic islet beta-cell line protects against cytokine-induced apoptosis and necrosis. Endocrinol. 2001; 142(8): 3649–3655.
50. Martínez-Castelao A, Hueso M, Sanz V, Rejas J, Alsina J, Grinyó JM. Treatment of hypertension after renal transplantation: long-term efficacy of verapamil, enalapril, and doxazosin. Kidney Int. 1998; 68: S130–S134.
51. de Cavanagh EM, Inserra F, Toblli J, Stella I, Fraga CG, Ferder L. Enalapril attenuates oxidative stress in diabetic rats. Hypertension 2001; 38: 1130–1136. doi: 10.1161/hy1101.092845 11711510
52. Hari P, Sahu J, Sinha A, Pandey RM, Bal CS, Bagga A. Effect of enalapril on glomerular filtration rate and proteinuria in children with chronic kidney disease: a randomized controlled trial. Ind Pediatr. 2013; 50: 923–928.
53. Björck S, Mulec H, Johnsen SA, Nordén G, Aurell M. Renal protective effect of enalapril in diabetic nephropathy. BMJ. 1992; 304: 339–343. doi: 10.1136/bmj.304.6823.339 1540729
54. Hou J, Yan G, Liu B, Zhu B, Qiao Y, Wang D, Li R, Luo E, Tang C. The protective effects of enalapril maleate and folic acid tablets against contrast-induced nephropathy in diabetic rats. Biomed Res Int. 2018; 2018: 4609750. doi: 10.1155/2018/4609750 29560361
55. Yang Z, Liu F, Qu H, Wang H, Xiao X, Deng H. 1,25(OH)2D3 protects β cell against high glucose-induced apoptosis through mTOR suppressing. Mol Cell Endocrinol. 2015; 414: 111–119 doi: 10.1016/j.mce.2015.07.023 26213322
56. Sanchez-Niño M, Bozic M, Córdoba-Lanús E, Valcheva P, Gracia O, Ibarz M, et al. Beyond proteinuria: VDR activation reduces renal inflammation in experimental diabetic nephropathy. Am J Physiol Renal Physiol. 2012; 302: F647–F657. doi: 10.1152/ajprenal.00090.2011 22169009
57. Tan X, Wen X, Liu Y. Paricalcitol inhibits renal inflammation by promoting vitamin D receptor-mediated sequestration of NF-kappaB signaling. J Am Soc Nephrol. 2008; 19: 1741–1752. doi: 10.1681/ASN.2007060666 18525004
58. He W, Kang YS, Dai C, Liu Y. Blockade of Wnt/beta-catenin signaling by paricalcitol ameliorates proteinuria and kidney injury. J Am Soc Nephrol. 2011; 22: 90–103. doi: 10.1681/ASN.2009121236 21030600
59. Chandran G, Sirajudeen KN, Yusoff NS, Swamy M, Samarendra MS. Effect of the antihypertensive drug enalapril on oxidative stress markers and antioxidant enzymes in kidney of spontaneously hypertensive rat. Oxid Med Cell Longev. 2014; Article ID 608512, 10 Pages.
60. Navarro JF, Milena FJ, Mora C, León C, Claverie F, Flores C, et al. Tumor necrosis factor-α gene expression in diabetic nephropathy: Relationship with urinary albumin excretion and effect of angiotensin-converting enzyme inhibition. Kidney Int. 2005; 68(99): S98–S102.
61. Kim JM, Heo HS, Choi YJ, Ye BH, Mi Ha Y, Seo AY, et al. Inhibition of NF-κB-induced inflammatory responses by angiotensin II antagonists in aged rat kidney. Exp Gerontol 2011; 46: 542–548. doi: 10.1016/j.exger.2011.02.011 21377515
62. Xin S, Yan H, Ma J, Sun Q, Shen L. Protective Effects of Luteolin on Lipopolysaccharide-Induced Acute Renal Injury in Mice. Med Sci Monit.: International Medical Journal of Experimental and Clinical Research. 2016; 22: 5173–5180.
63. Li YC, Kong J, Wei M, Chen ZF, Liu SQ, Cao LP. 1,25-Dihydroxyvitamin D(3) is a negative endocrine regulator of the renin-angiotensin system. J Clin Invest. 2002; 110: 229–238. doi: 10.1172/JCI15219 12122115
64. Sznarkowska A, Olszewski R, Zawacka-Pankau J. Farmakologiczna aktywacja supresora nowotworu, natywnego białka p53 jako obiecująca strategia zwalczania nowotworów. [Pharmacological activation of tumor suppressor, wild-type p53 as a promising strategy to fight cancer] (in Polish) Postepy Hig. Med. Dośw (online) 2010; 64: 396–407.
65. Stennicke HR, Salvesen GS. Biochemical characteristics of caspases-3, -6, -7, and -8. J Biol Chem. 1997; 272 (41): 25719–23. doi: 10.1074/jbc.272.41.25719 9325297
66. Ghavami S, Hashemi M, Ande SR, Yeganeh B, Xiao W, Eshraghi M, et al. Apoptosis and cancer: mutations within caspase genes. J Med Genet. 2009; 46 (8): 497–510. doi: 10.1136/jmg.2009.066944 19505876
67. Jones BE, Lo CR, Liu H, Srinivasan A, Streetz K, Valentino KL et al. Hepatocytes sensitized to tumor necrosis factor-α cytotoxicity undergo apoptosis through caspase-dependent and caspase-independent pathways. J Biol Chem. 2000; 275: 705–712. doi: 10.1074/jbc.275.1.705 10617670
68. El-Beshbishy HA, Bahashwan SA, Aly HA, Fakher HA. Abrogation of cisplatin-induced nephrotoxicity in mice by alpha lipoic acid through ameliorating oxidative stress and enhancing gene expression of antioxidant enzymes. Eur J Pharmacol. 2011; 668: 278–284. doi: 10.1016/j.ejphar.2011.06.051 21763304
69. Zhang C, Wu L, Tashiro S, Onodera S, Ikejima T. Oridonin induces apoptosis of Hela cells via altering expression of Bcl-2/Bax and activating caspase-3/ICAD pathway. Acta Pharmacol Sin. 2004; 25: 691–698. 15132839
70. Rani N, Bharti S, Tomar A, Dinda AK, Arya DS, Bhatia J et al. Inhibition of PARP activation by enalapril is crucial for its renoprotective effect in cisplatin-induced nephrotoxicity in rats. Free Radical Res. 2016; 50 (11): 1226–1236.
71. Park JW, Cho JW, Joo SY, Kim CS, Choi JS, Bae EH, Ma SK, et al. Paricalcitol prevents cisplatin-induced renal injury by suppressing apoptosis and proliferation. Eur J Pharmacol. 2012; 683: 301–309. doi: 10.1016/j.ejphar.2012.03.019 22449373
72. Suh SH, Lee KE, Park JW, Kim IJ, Kim O, Kim CS et al. Antiapoptotic effect of paricalcitol in gentamicin-induced kidney injury. Korean J Physiol Pharmacol. 2013; 17: 435–440. doi: 10.4196/kjpp.2013.17.5.435 24227945
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