Protective effects of enalapril in streptozotocin-induced diabetic rat: Studies of DNA damage, apoptosis and expression of CCN2 in the heart, kidney and liver

Journal of Applied Toxicology

Volumn 32, Issue 9, 2012, Pages 662-672

  Kushwaha, S ^a   Vikram, A ^a   Jena, G B ^a  

^a NATIONAL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH NIPER   (India)

Author keywords

CCN2; Comet assay; Diabetes; DNA damage; Enalapril

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; ENALAPRIL; GLUTATHIONE; MALONALDEHYDE; STREPTOZOCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DRUG EFFECT; DRUG EFFICACY; FIBROSIS; HEART; HEART PROTECTION; KIDNEY; LIVER; LIVER PROTECTION; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RENAL PROTECTION; STREPTOZOCIN DIABETES;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; APOPTOSIS; COMET ASSAY; CONNECTIVE TISSUE GROWTH FACTOR; DIABETES MELLITUS, EXPERIMENTAL; DNA DAMAGE; ENALAPRIL; FIBROSIS; HEART; KIDNEY; LIVER; MALE; MYOCARDIUM; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; STREPTOZOCIN;

ANIMALIA; RATTUS;

EID: 84864322238     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.1670     Document Type: Article

References (45)

1. Anderson B, Khaper N, Dhalla AK, Singal PK. 1996. Anti-free radical mechanisms in captopril protection against reperfusion injury in isolated rat hearts. Can. J. Cardiol. 12(10): 1099-1104.
2. Aragno M, Mastrocola R, Alloatti G, Vercellinatto I, Bardini P, Geuna S, Catalano MG, Danni O, Boccuzzi G. 2008. Oxidative stress triggers cardiac fibrosis in the heart of diabetic rats. Endocrinology 149(1): 380-388.
3. Arun KH, Kaul CL, Ramarao P. 2005. AT1 receptors and L-type calcium channels: functional coupling in supersensitivity to angiotensin II in diabetic rats. Cardiovasc. Res. 65(2): 374-386.
4. Bain SC, Le Guen CA, Lunec J, Barnett AH. 1991. Comparison of the free radical scavenging activity of captopril versus enalapril: a three month in vivo study in hypertensive diabetic patients. J. Human Hyper. 5(6): 511-515.
5. Baluchnejadmojarad T, Roghani M, Imani A. 2004. Protective effect of enalapril on vascular reactivity of the rat aorta. Vascul. Pharmacol. 40(6): 301-307.
6. Ban CR, Twigg SM. 2008. Fibrosis in diabetes complications: pathogenic mechanisms and circulating and urinary markers. Vasc. Health Risk Mgmt 4(3): 575-596.
7. Barber DA, Harris SR. 1994. Oxygen free radicals and antioxidants: a review. Am. Pharm. NS34(9): 26-35.
8. Baynes JW, Thorpe SR. 1999. Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 48(1): 1-9.
9. Cagalinec M, Kyselovic J, Blaskova E, Bacharova L, Chorvat D, Jr., Chorvatova A. 2006. Comparative study of the effects of lacidipine and enalapril on the left ventricular cardiomyocyte remodeling in spontaneously hypertensive rats. J. Cardiovasc. Pharmacol. 47(4): 561-570.
10. Cardin S, Li D, Thorin-Trescases N, Leung TK, Thorin E, Nattel S. 2003. Evolution of the atrial fibrillation substrate in experimental congestive heart failure: angiotensin-dependent and -independent pathways. Cardiovasc. Res. 60(2): 315-325.
11. Chen SX, Song T, Zhou SH, Liu YH, Wu SJ, Liu LY. 2008. Protective effects of ACE inhibitors on vascular endothelial dysfunction induced by exogenous advanced oxidation protein products in rats. Eur. J. Pharmacol. 584(2-3): 368-375.
12. Choucroun P, Gillet D, Dorange G, Sawicki B, Dewitte JD. 2001. Comet assay and early apoptosis. Mutat. Res. 478(1-2): 89-96.
13. Collins AR, Duthie SJ, Dobson VL. 1993. Direct enzymic detection of endogenous oxidative base damage in human lymphocyte DNA. Carcinogenesis 14(9): 1733-2735.
14. Costa JC, Costa RS, Silva CG, Coimbra TM. 2006. Enalapril reduces the expression of nuclear factor-kappaB and c-Jun N-terminal kinase in the renal cortices of five-sixths-nephrectomized rats. Am. J. Nephrol. 26(3): 281-286.
15. de Cavanagh EM, Inserra F, Ferder L, Romano L, Ercole L, Fraga CG. 1995. Superoxide dismutase and glutathione peroxidase activities are increased by enalapril and captopril in mouse liver. FEBS Lett. 361(1): 22-24.
16. de Cavanagh EM, Inserra F, Ferder L, Fraga CG. 2000. Enalapril and captopril enhance glutathione-dependent antioxidant defenses in mouse tissues. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278(3): R572-R577.
17. de Cavanagh EM, Flores I, Ferder M, Inserra F, Ferder L. 2008. Renin-angiotensin system inhibitors protect against age-related changes in rat liver mitochondrial DNA content and gene expression. Exp. Gerontol. 43(10): 919-928.
18. Duarte J, Martinez A, Bermejo A, Vera B, Gamez MJ, Cabo P, Zarzuelo A. 1999. Cardiovascular effects of captopril and enalapril in obese Zucker rats. Eur. J. Pharmacol. 365(2-3): 225-232.
19. Ferder L, Inserra F, Romano L, Ercole L, Pszenny V. 1993. Effects of angiotensin-converting enzyme inhibition on mitochondrial number in the aging mouse. Am. J. Physiol. 265(1 Pt 1): C15-18.
20. Ghorbanihaghjo A, Veisi P, Argani H, Aghaeishahsavari M, Noroozianavval M, Rashtchizadeh N, Mesgari M, Safa J, Babaei H. 2008. Prevention of DNA damage in renal transplantation by losartan and enalapril: the role of renin-angiotensin system polymorphisms. Clin. Exp. Nephrol. 12(1): 65-73.
21. Gupta S, Clarkson MR, Duggan J, Brady HR. 2000. Connective tissue growth factor: potential role in glomerulosclerosis and tubulointerstitial fibrosis. Kidney Int. 58(4): 1389-1399.
22. Husain K, Ferder L, Mizobuchi M, Finch J, Slatopolsky E. 2009. Combination therapy with paricalcitol and enalapril ameliorates cardiac oxidative injury in uremic rats. Am. J. Nephrol. 29(5): 465-472.
23. Kaminski KA, Szepietowska B, Bonda T, Kozuch M, Mencel J, Malkowski A, Sobolewski K, Kovalchuk O, Chyczewski L, Szelachowska M et al. 2009. CCN2 protein is an announcing marker for cardiac remodeling following STZ-induced moderate hyperglycemia in mice. Pharmacol. Rep. 61(3): 496-503.
24. Klaunig JE, Kamendulis LM. 2004. The role of oxidative stress in carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 44: 239-267.
25. Li Y, Samuvel DJ, Sundararaj KP, Lopes-Virella MF, Huang Y. 2010. IL-6 and high glucose synergistically upregulate MMP-1 expression by U937 mononuclear phagocytes via ERK1/2 and JNK pathways and c-Jun. J. Cell Biochem. 110(1): 248-259.
26. Lima PH, Sinzato YK, de Souza Mda S, Braz MG, Rudge MV, Damasceno DC. 2007. Evaluation of level of DNA damage in blood leukocytes of non-diabetic and diabetic rat exposed to cigarette smoke. Mutat. Res. 628(2): 117-122.
27. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193(1): 265-275.
28. Moron MS, Depierre JW, Mannervik B. 1979. Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim. Biophys. Acta 582(1): 67-78.
29. Ohkawa H, Ohishi N, Yagi K. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95(2): 351-358.
30. Przyklenk K, Kloner RA. 1991. Angiotensin converting enzyme inhibitors improve contractile function of stunned myocardium by different mechanisms of action. Am. Heart J. 121(5): 1319-1330.
31. Riser BL, Najmabadi F, Perbal B, Rambow JA, Riser ML, Sukowski E, Yeger H, Riser SC, Peterson DR. 2010. CCN3/CCN2 regulation and the fibrosis of diabetic renal disease. J. Cell Commun. Signal. 4(1): 39-50.
32. Roestenberg P, van Nieuwenhoven FA, Joles JA, Trischberger C, Martens PP, Oliver N, Aten J, Hoppener JW, Goldschmeding R. 2006. Temporal expression profile and distribution pattern indicate a role of connective tissue growth factor (CTGF/CCN-2) in diabetic nephropathy in mice. Am. J. Physiol. Renal Physiol. 290(6): F1344-F1354.
33. Roser S, Pool-Zobel BL, Rechkemmer G. 2001. Contribution of apoptosis to responses in the comet assay. Mutat. Res. 497(1-2): 169-175.
34. Schmid U, Stopper H, Schweda F, Queisser N, Schupp N. 2008. Angiotensin II induces DNA damage in the kidney. Cancer Res. 68(22): 9239-9246.
35. Singh NP, McCoy MT, Tice RR, Schneider EL. 1988. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 175(1): 184-191.
36. Tam FW, Riser BL, Meeran K, Rambow J, Pusey CD, Frankel AH. 2009. Urinary monocyte chemoattractant protein-1 (MCP-1) and connective tissue growth factor (CCN2) as prognostic markers for progression of diabetic nephropathy. Cytokine 47(1): 37-42.
37. Tripathi DN, Jena GB. 2009. Intervention of astaxanthin against cyclophosphamide-induced oxidative stress and DNA damage: a study in mice. Chem. Biol. Interact. 180(3): 398-406.
38. Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J. 2004. Role of oxygen radicals in DNA damage and cancer incidence. Mol. Cell Biochem. 266(1-2): 37-56.
39. Vikram A, Tripathi DN, Ramarao P, Jena GB. 2008. Intervention of D-glucose ameliorates the toxicity of streptozotocin in accessory sex organs of rat. Toxicol. Appl. Pharmacol. 226(1): 84-93.
40. Wang B, Carter RE, Jaffa MA, Nakerakanti S, Lackland D, Lopes-Virella M, Trojanowska M, Luttrell LM, Jaffa AA. 2010. Genetic variant in the promoter of connective tissue growth factor gene confers susceptibility to nephropathy in type 1 diabetes. J. Med. Genet. 47(6): 391-397.
41. Wang X, McLennan SV, Allen TJ, Tsoutsman T, Semsarian C, Twigg SM. 2009. Adverse effects of high glucose and free fatty acid on cardiomyocytes are mediated by connective tissue growth factor. Am. J. Physiol. Cell Physiol. 297(6): C1490-1500.
42. WHO. 1999. Definition, Diagnosis and Classification of Diabetes Mellitus and its Complications. Report of a WHO Consultation Part 1. WHO: Geneva; 1-59.
43. Yamazaki T, Tanimoto M, Gohda T, Ohara I, Hagiwara S, Murakoshi M, Matsumoto M, Kaneko S, Aoki T, Toyoda H et al. 2009. Combination effects of enalapril and losartan on lipid peroxidation in the kidneys of KK-Ay/Ta mice. Nephron Exp. Nephrol. 113(2): e66-e76.
44. Yokoi H, Mukoyama M, Mori K, Kasahara M, Suganami T, Sawai K, Yoshioka T, Saito Y, Ogawa Y, Kuwabara T et al. 2008. Overexpression of connective tissue growth factor in podocytes worsens diabetic nephropathy in mice. Kidney Int. 73(4): 446-455.
45. Zhang BQ, Huang YS, Zhang JP, Zhang DX, Dang YM, Wang G, Hu JY, Lei ZY, Xiao R. 2007. Protective effects of administration of enalapril maleate on rat myocardial damage in early stage of burns. Zhonghua Shao Shang Za Zhi 23(5): 335-338.