Angiotensin-converting enzyme inhibition and angiotensin AT1 receptor blockade downregulate angiotensin-converting enzyme expression and attenuate renal injury in streptozotocin-induced diabetic rats

Journal of Biochemical and Molecular Toxicology

Volumn 27, Issue 7, 2013, Pages 378-387

  Motawi, Tarek K ^a   El Maraghy, Shohda A ^a   Senousy, Mahmoud A ^a  

^a CAIRO UNIVERSITY   (Egypt)

Author keywords

ACE expression; ACE inhibitor; AT1 receptor blocker; Diabetic nephropathy; Na+ K+ ATPase; Oxidative stress

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ANGIOTENSIN 1 RECEPTOR; CREATININE; DIPEPTIDYL CARBOXYPEPTIDASE; ENALAPRIL; GLUCOSE; HEMOGLOBIN A1C; NITRATE; NITRITE; POTASSIUM; SODIUM; STREPTOZOCIN; TRANSFORMING GROWTH FACTOR BETA1; VALSARTAN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; ENZYME ACTIVITY; ENZYME INHIBITION; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY MASS; KIDNEY STRUCTURE; MALE; MICROALBUMINURIA; NONHUMAN; OXIDATIVE STRESS; POTASSIUM BLOOD LEVEL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SODIUM BLOOD LEVEL; STREPTOZOCIN DIABETES; TREATMENT DURATION;

ACE EXPRESSION; ACE INHIBITOR; AT1 RECEPTOR BLOCKER; DIABETIC NEPHROPATHY; NA+/K+-ATPASE; OXIDATIVE STRESS;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; ENALAPRIL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; KIDNEY; MALE; PEPTIDYL-DIPEPTIDASE A; RATS; RATS, WISTAR; RECEPTOR, ANGIOTENSIN, TYPE 1; TETRAZOLES; TRANSFORMING GROWTH FACTOR BETA1; VALINE;

RATTUS; RATTUS NORVEGICUS;

EID: 84879846047     PISSN: 10956670     EISSN: 10990461     Source Type: Journal    
DOI: 10.1002/jbt.21500     Document Type: Article

References (53)

1. Stanton RC, King GL. A complex interplay of factors causes diabetic nephropathy. Metabolism 2011;60:591-593.
2. Balakumar P, Chakkarwar VA, Krishan P, Singh M. Vascular endothelial dysfunction: a tug of war in diabetic nephropathy? Biomed Pharmacother 2009;63:171-179.
3. Carey RM, Siragy HM. The intrarenal renin-angiotensin system and diabetic nephropathy. Trends Endocrinol Metab 2003;14:274-281.
4. Lai KN, Leung JC, Tang SC. The renin-angiotensin system. Contrib Nephrol 2011;170:135-144.
5. Lely AT, Luik PT, Navis G. Angiotensin I-converting enzyme: a pathogenetic role in diabetic renal damage? Curr Diabetes Rev 2007;3:41-52.
6. Mimouni S, Raffaitin C, Corcuff JB. Ac-SDKP, a marker of the angiotensin-converting enzyme activity? Ann Biol Clin 2006;64:11-16.
7. Kobori H, Nangaku M, Navar LG, Nishiyama A. The intrarenal renin-angiotensin system: from physiology to the pathobiology of hypertension and kidney disease. Pharmacol Rev 2007;59:251-287.
8. Kobori H, Ozawa Y, Suzaki Y, Prieto-Carrasquero MC, Nishiyama A, Shoji T, Cohen EP, Navar LG. Young Scholars Award Lecture: Intratubular angiotensinogen in hypertension and kidney diseases. Am J Hypertens 2006;19:541-550.
9. Mezzano S, Droguett A, Burgos ME, Ardiles LG, Flores CA, Aros CA, Caorsi I, Vio CP, Ruiz-Ortega M, Egido J. Renin-angiotensin system activation and interstitial inflammation in human diabetic nephropathy. Kidney Int Suppl 2003;86:S64-S70.
10. Konoshita T, Wakahara S, Mizuno S, Motomura M, Aoyama C, Makino Y, Kawai Y, Kato N, Koni I, Miyamori I, Mabuchi H. Tissue gene expression of renin-angiotensin system in human type 2 diabetic nephropathy. Diabetes Care 2006;29:848-852.
11. Wolf G. Renal injury due to renin-angiotensin-aldosterone system activation of the transforming growth factor-beta pathway. Kidney Int 2006;70:1914-1919.
12. Russo LM, del Re E, Brown D, Lin HY. Evidence for a role of transforming growth factor (TGF)-beta1 in the induction of postglomerular albuminuria in diabetic nephropathy: amelioration by soluble TGF-beta type II receptor. Diabetes 2007;56:380-388.
13. Fekete A, Rosta K, Wagner L, Prokai A, Degrell P, Ruzicska E, Vegh E, Toth M, Ronai K, Rusai K, Somogyi A, Tulassay T, Szabo AJ, Ver A. Na+, K+-ATPase is modulated by angiotensin II in diabetic rat kidney-another reason for diabetic nephropathy? J Physiol 2008;586:5337-5348.
14. Kedziora-Kornatowska KZ, Luciak M, Paszkowski J. Lipid peroxidation and activities of antioxidant enzymes in the diabetic kidney: effect of treatment with angiotensin convertase inhibitors. IUBMB Life 2000;49:303-307.
15. Lopez B, Salom MG, Arregui B, Valero F, Fenoy FJ. Role of superoxide in modulating the renal effects of angiotensin II. Hypertension 2003;42:1150-1156.
16. Komers R, Anderson S. Paradoxes of nitric oxide in the diabetic kidney. Am J Physiol Renal Physiol 2003;284:F1121-1137.
17. Ferrario CM, Jessup J, Chappell MC, Averill DB, Brosnihan KB, Tallant EA, Diz DI, Gallagher PE. Effect of angiotensin-converting enzyme inhibition and angiotensin II receptor blockers on cardiac angiotensin-converting enzyme 2. Circulation 2005;111:2605-2610.
18. Ripley E. Complementary effects of angiotensin-converting enzyme inhibitors and angiotensin receptor blockers in slowing the progression of chronic kidney disease. Am Heart J 2009;157(Suppl 6):S7-S16.
19. Mogensen CE, Cooper ME. Diabetic renal disease: from recent studies to improved clinical practice. Diabet Med 2004;21:4-17.
20. Sen S, Kanter M, Ustundag S, Aktas C, Dogutan H, Yalcin O. Effect of angiotensin-converting enzyme inhibition and angiotensin II type 1 receptor blockade on streptozotocin-induced diabetic nephropathy. Ren Fail 2008;30:1023-1033.
21. Kalender B, Ozturk M, Tuncdemir M, Uysal O, Dagistanli FK, Yegenaga I, Erek E. Renoprotective effects of valsartan and enalapril in STZ-induced diabetes in rats. Acta Histochem 2002;104:123-130.
22. Peters H, Border WA, Noble NA. Targeting TGF-beta overexpression in renal disease: maximizing the antifibrotic action of angiotensin II blockade. Kidney Int 1998;54:1570-1580.
23. Tominaga N, Robert A, Izuhara Y, Ohtomo S, Dan T, Chihara K, Kurokawa K, Van Ypersele de Strihou C, Miyata T. Very high doses of valsartan provide renoprotection independently of blood pressure in a type 2 diabetic nephropathy rat model. Nephrology (Carlton) 2009;14:581-587.
24. Gu C, Zhou G, Noble NA, Border WA, Cheung AK, Huang Y. Targeting reduction of proteinuria in glomerulonephritis: Maximizing the antifibrotic effect of valsartan by protecting podocytes. J Renin Angiotensin Aldosterone Syst 2012, DOI:10.1177/1470320312466127.
25. Mavrakanas TA, Cheva A, Kallaras K, Karkavelas G, Mironidou-Tzouveleki M. Effect of ramipril alone compared to ramipril with eplerenone on diabetic nephropathy in streptozocin-induced diabetic rats. Pharmacology 2010;86:85-91.
26. Knoll E, Wisser H, Rautenstrauch H. [Comparative study of the diagnostic value of disc electrophoresis of urinary proteins and measurement of the excretion of N-acetylglucosaminidase for the detection of renal tubule damage in chronic polyarthritis (author's transl)]. J Clin Chem Clin Biochem 1980;18:53-58.
27. Wehbi GJ, Zimpelmann J, Carey RM, Levine DZ, Burns KD. Early streptozotocin-diabetes mellitus downregulates rat kidney AT2 receptors. Am J Physiol Renal Physiol 2001;280:F254-265.
28. Angele P, Abke J, Kujat R, Faltermeier H, Schumann D, Nerlich M, Kinner B, Englert C, Ruszczak Z, Mehrl R, Mueller R. Influence of different collagen species on physico-chemical properties of crosslinked collagen matrices. Biomaterials 2004;25:2831-2841.
29. Woessner JF, Jr. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys 1961;93:440-447.
30. Rasch R. Kidney Na, K-ATPase activity in streptozotocin-diabetic rats. Scand J Clin Lab Invest 1986;46:59-62.
31. Weidman S, Schonfels G. Lipids and Lipoproteins. In: Sonnenwirth AC, Jarett L, editors. Gradwohl's clinical laboratory methods and diagnosis. St. Louis, MO: Mosby; 1980. pp 272-304.
32. Miranda KM, Espey MG, Wink DA. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 2001;5:62-71.
33. Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 1978;86:271-278.
34. Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys 1959;82:70-77.
35. Engelhardt G, Homma D. Effects of acetylsalicylic acid, paracetamol and caffeine and a combination of these substances on kidney glutathione levels. Arzneimittelforschung 1996;46:513-518.
36. Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967;70:158-169.
37. Zaheer N, Tewari KK, Krishnan PS. Exposure and solubilization of hepatic mitochondrial shunt dehydrogenases. Arch Biochem Biophys 1965;109:646-648.
38. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-275.
39. Banchroft J, Stevens A, Turner D. Theory and practice of histological techniques, 4th edn. New York: Churchil Livingstone; 1996. pp 125.
40. Koka V, Huang XR, Chung AC, Wang W, Truong LD, Lan HY. Angiotensin II up-regulates angiotensin I-converting enzyme (ACE), but down-regulates ACE2 via the AT1-ERK/p38 MAP kinase pathway. Am J Pathol 2008;172:1174-1183.
41. 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(Suppl 1):S42-45.
42. Thomas MC, Tikellis C, Burns WM, Bialkowski K, Cao Z, Coughlan MT, Jandeleit-Dahm K, Cooper ME, Forbes JM. Interactions between renin angiotensin system and advanced glycation in the kidney. J Am Soc Nephrol 2005;16:2976-2984.
43. Hsieh TJ, Fustier P, Wei CC, Zhang SL, Filep JG, Tang SS, Ingelfinger JR, Fantus IG, Hamet P, Chan JS. Reactive oxygen species blockade and action of insulin on expression of angiotensinogen gene in proximal tubular cells. J Endocrinol 2004;183:535-550.
44. Zhang Y, Bloem LJ, Yu L, Estridge TB, Iversen PW, McDonald CE, Schrementi JP, Wang X, Vlahos CJ, Wang J. Protein kinase C beta II activation induces angiotensin converting enzyme expression in neonatal rat cardiomyocytes. Cardiovasc Res 2003;57:139-146.
45. Kohlstedt K, Brandes RP, Muller-Esterl W, Busse R, Fleming I. Angiotensin-converting enzyme is involved in outside-in signaling in endothelial cells. Circ Res 2004;94:60-67.
46. Ostergren J. Renin-angiotensin-system blockade in the prevention of diabetes. Diabetes Res Clin Pract 2007;76(Suppl 1):S13-S21.
47. Hill C, Logan A, Smith C, Gronbaek H, Flyvbjerg A. Angiotensin converting enzyme inhibitor suppresses glomerular transforming growth factor beta receptor expression in experimental diabetes in rats. Diabetologia 2001;44:495-500.
48. Shibuya K, Kanasaki K, Isono M, Sato H, Omata M, Sugimoto T, Araki S, Isshiki K, Kashiwagi A, Haneda M, Koya D. N-acetyl-seryl-aspartyl-lysyl-proline prevents renal insufficiency and mesangial matrix expansion in diabetic db/db mice. Diabetes 2005;54:838-845.
49. 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;61:186-194.
50. Kedziora-Kornatowska K. Effect of angiotensin convertase inhibitors and AT1 angiotensin receptor antagonists on the development of oxidative stress in the kidney of diabetic rats. Clin Chim Acta 1999;287:19-27.
51. Andersson RM, Aizman O, Aperia A, Brismar H. Modulation of Na+, K+-ATPase activity is of importance for RVD. Acta Physiol Scand 2004;180:329-334.
52. Banday AA, Lokhandwala MF. Loss of biphasic effect on Na/K-ATPase activity by angiotensin II involves defective angiotensin type 1 receptor-nitric oxide signaling. Hypertension 2008;52:1099-1105.
53. Azuma KK, Hensley CB, Tang MJ, McDonough AA. Thyroid hormone specifically regulates skeletal muscle Na(+)-K(+)-ATPase alpha 2- and beta 2-isoforms. Am J Physiol 1993;265:C680-687.