Spironolactone improves endothelial dysfunction in streptozotocin-induced diabetic rats

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 387, Issue 12, 2014, Pages 1187-1197

  Adel, Heba ^a   Taye, Ashraf ^a   Khalifa, Mohamed M A ^a  

^a Minia University   (Egypt)

Author keywords

Diabetes; Endothelial dysfunction; Oxidative stress; Spironolactone; Streptozotocin

Indexed keywords

3,4 METHYLENEDIOXYAMPHETAMINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; NITRIC OXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SPIRONOLACTONE; TRANSFORMING GROWTH FACTOR BETA; ANTIOXIDANT; MALONALDEHYDE; MINERALOCORTICOID ANTAGONIST; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; BIOAVAILABILITY; BLOOD VESSEL REACTIVITY; BODY WEIGHT; CELL VACUOLE; CONTROLLED STUDY; DIABETIC ANGIOPATHY; ENDOTHELIAL DYSFUNCTION; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; IMMUNOREACTIVITY; LIPID PEROXIDATION; MALE; NONHUMAN; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; RAT; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; UPREGULATION; ANIMAL; AORTA; COMPLICATION; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC ANGIOPATHIES; DRUG EFFECTS; METABOLISM; ORAL DRUG ADMINISTRATION; PATHOLOGY; VASCULAR ENDOTHELIUM; WISTAR RAT;

ADMINISTRATION, ORAL; ANIMALS; ANTIOXIDANTS; AORTA; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC ANGIOPATHIES; ENDOTHELIUM, VASCULAR; MALE; MALONDIALDEHYDE; MINERALOCORTICOID RECEPTOR ANTAGONISTS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, WISTAR; SPIRONOLACTONE; STREPTOZOCIN;

EID: 84922002850     PISSN: 00281298     EISSN: 14321912     Source Type: Journal    
DOI: 10.1007/s00210-014-1048-3     Document Type: Article

References (53)

1. Ajay M, Achike FI, Mustafa AM, Mustafa MR (2006) Effect of quercetin on altered vascular reactivity in aortas isolated from streptozotocin-induced diabetic rats. Diabetes Res Clin Pract 73:1-7
2. Bauersachs J, Heck M, Fraccarollo D, Hildemann SK, Ertl G, Wehling M, Christ M (2002) Addition of spironolactone to angiotensin-converting enzyme inhibition in heart failure improves endothelial vasomotor dysfunction: role of vascular superoxide anion formation and endothelial nitric oxide synthase expression. J Am Coll Cardiol 39:351-358
3. Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245-313
4. Benetos A, Lacolley P, Safar ME (1997) Prevention of aortic fibrosis by spironolactone in spontaneously hypertensive rats. Arterioscler Thromb Vasc Biol 17:1152-1156
5. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302-310
6. Buikema H, Monnink SH, Tio RA, Crijns HJ, de Zeeuw D, van Gilst WH (2000) Comparison of zofenopril and lisinopril to study the role of the sulfhydryl-group in improvement of endothelial dysfunction with ACE-inhibitors in experimental heart failure. Br J Pharmacol 130:1999-2007
7. Cangemi R, Pignatelli P, Carnevale R, Nigro C, Proietti M, Angelico F, Lauro D, Basili S, Violi F (2012) Platelet isoprostane overproduction in diabetic patients treated with aspirin. Diabetes 61:1626-1632
8. Chen B, Zhao Q, Ni R, Tang F, Shan L, Cepinskas I, Cepinskas G, Wang W, Schiller PW, Peng T (2014) Inhibition of calpain reduces oxidative stress and attenuates endothelial dysfunction in diabetes. Cardiovasc Diabetol 13:88-99
9. Cheng YS, Dai DZ, Dai Y (2013) AQP4 KO exacerbating renal dysfunction is mediated by endoplasmic reticulum stress and p66Shc and is attenuated by apocynin and endothelin antagonist CPU0213. Eur J Pharmacol 721:249-258
10. Cosentino F, Hishikawa K, Katusic ZS, Luscher TF (1997) High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation 96:25-28
11. Creager MA, Luscher TF, Cosentino F, Beckman JA (2003) Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: Part I. Circulation 108:1527-1532
12. Dahiya R, Lin A, Bakircioglu ME, Huang ST, Lue TF (1997) mRNA and protein expression of nitric oxide synthase and adrenoceptor alpha 1 in young and old rat penile tissues. Br J Urol 80:300-306
13. Dixon IM, Hao J, Reid NL, Roth JC (2000) Effect of chronic AT(1) receptor blockade on cardiac Smad overexpression in hereditary cardiomyopathic hamsters. Cardiovasc Res 46:286-297
14. El-Remessy AB, Abou-Mohamed G, Caldwell RW, Caldwell RB (2003) High glucose-induced tyrosine nitration in endothelial cells: role of eNOS uncoupling and aldose reductase activation. Invest Ophthalmol Vis Sci 44:3135-3143
15. Farquharson CA, Struthers AD (2000) Spironolactone increases nitric oxide bioactivity, improves endothelial vasodilator dysfunction, and suppresses vascular angiotensin I/angiotensin II conversion in patients with chronic heart failure. Circulation 101:594-597
16. Giugliano D, Ceriello A, Paolisso G (1996) Oxidative stress and diabetic vascular complications. Diabetes Care 19:257-267
17. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 126:131-138
18. Gryglewski RJ, Palmer RM, Moncada S (1986) Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 320:454-456
19. Guo C, Martinez-Vasquez D, Mendez GP, Toniolo MF, Yao TM, Oestreicher EM, Kikuchi T, Lapointe N, Pojoga L, Williams GH, Ricchiuti V, Adler GK (2006) Mineralocorticoid receptor antagonist reduces renal injury in rodent models of types 1 and 2 diabetes mellitus. Endocrinology 147:5363-5373
20. Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M (1998) Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 339:229-234
21. Han KH, Kang YS, Han SY, Jee YH, Lee MH, Han JY, Kim HK, Kim YS, Cha DR (2006) Spironolactone ameliorates renal injury and connective tissue growth factor expression in type II diabetic rats. Kidney Int 70:111-120
22. Jaffe IZ, Mendelsohn ME (2005) Angiotensin II and aldosterone regulate gene transcription via functional mineralocortocoid receptors in human coronary artery smooth muscle cells. Circ Res 96:643-650
23. Kazuyama E, Saito M, Kinoshita Y, Satoh I, Dimitriadis F, Satoh K (2009) Endothelial dysfunction in the early- and late-stage type-2 diabetic Goto-Kakizaki rat aorta. Mol Cell Biochem 332:95-102
24. Kushibiki M, Yamada M, Oikawa K, Tomita H, Osanai T, Okumura K (2007) Aldosterone causes vasoconstriction in coronary arterioles of rats via angiotensin II type-1 receptor: influence of hypertension. Eur J Pharmacol 572:182-188
25. Losel R, Schultz A, Boldyreff B, Wehling M (2004) Rapid effects of aldosterone on vascular cells: clinical implications. Steroids 69:575-578
26. Matsumoto T, Ishida K, Nakayama N, Taguchi K, Kobayashi T, Kamata K (2010) Mechanisms underlying the losartan treatment-induced improvement in the endothelial dysfunction seen in mesenteric arteries from type 2 diabetic rats. Pharmacol Res 62:271-281
27. Matsumoto S, Gotoh N, Hishinuma S, Abe Y, Shimizu Y, Katano Y, Ishihata A (2014) The role of hypertriglyceridemia in the development of atherosclerosis and endothelial dysfunction. Nutrients 6:1236-1250
28. Miric G, Dallemagne C, Endre Z, Margolin S, Taylor SM, Brown L (2001) Reversal of cardiac and renal fibrosis by pirfenidone and spironolactone in streptozotocin-diabetic rats. Br J Pharmacol 133:687-694
29. Mollnau H, Oleze M, Zinßius E, Hausding M, Wu Z, Knorr M, Ghaemi Kerahodi J, Kröller-Schön S, Jansen T, Teutsch C, Foster C, Li H, Wenzel P, Schulz E, Münzel T, Daiber A (2013) Effects of telmisartan or amlodipine monotherapy versus telmisartan/amlodipine combination therapy on vascular dysfunction and oxidative stress in diabetic rats. Naunyn Schmiedeberg's Arch Pharmacol 386:405-419
30. Nagatomo Y, Meguro T, Ito H, Koide K, Anzai T, Fukuda K, Ogawa S, Yoshikawa T (2014) Significance of AT1 receptor independent activation of mineralocorticoid receptor in murine diabetic cardiomyopathy. PLoS One 9:e93145
31. Oberleithner H (2005) Aldosterone makes human endothelium stiff and vulnerable. Kidney Int 67:1680-1682
32. Oelze M, Schuhmacher S, Daiber A (2010) Organic nitrates and nitrate resistance in diabetes: the role of vascular dysfunction and oxidative stress with emphasis on antioxidant properties of pentaerithrityl tetranitrate. Exp Diabetes Res 2010:213176
33. Oelze M, Knorr M, Knorr M, Schuhmacher S, Heeren T, Otto C, Schulz E, Reifenberg K, Wenzel P, Munzel T, Daiber A (2011) Vascular dysfunction in streptozotocin-induced experimental diabetes strictly depends on insulin deficiency. J Vasc Res 48:275-284
34. Okon EB, Chung AW, Rauniyar P, Padilla E, Tejerina T, McManus BM, Luo H, van Breemen C (2005) Compromised arterial function in human type 2 diabetic patients. Diabetes 54:2415-2423
35. Otani H, Otsuka F, Inagaki K, Suzuki J, Miyoshi T, Kano Y, Goto J, Ogura T, Makino H (2008) Aldosterone breakthrough caused by chronic blockage of angiotensin II type 1 receptors in human adrenocortical cells: possible involvement of bone morphogenetic protein-6 actions. Endocrinology 149:2816-2825
36. Oyadomari S, Gotoh T, Aoyagi K, Araki E, Shichiri M, Mori M (2001) Coinduction of endothelial nitric oxide synthase and arginine recycling enzymes in aorta of diabetic rats. Nitric Oxide 5:252-260
37. Park JB, Schiffrin EL (2002) Cardiac and vascular fibrosis and hypertrophy in aldosterone-infused rats: role of endothelin-1. Am J Hypertens 15:164-169
38. Pessoa BS, Peixoto EB, Papadimitriou A, Lopes de Faria JM, Lopes de Faria JB (2012) Spironolactone improves nephropathy by enhancing glucose-6-phosphate dehydrogenase activity and reducing oxidative stress in diabetic hypertensive rat. J Renin-Angiotensin-Aldosterone Syst 13:56-66
39. Rajagopalan S, Duquaine D, King S, Pitt B, Patel P (2002) Mineralocorticoid receptor antagonism in experimental atherosclerosis. Circulation 105:2212-2216
40. Schafer A, Fraccarollo D, Hildemann SK, Tas P, Ertl G, Bauersachs J (2003) Addition of the selective aldosterone receptor antagonist eplerenone to ACE inhibition in heart failure: effect on endothelial dysfunction. Cardiovasc Res 58:655-662
41. Schiffrin EL, Touyz RM (2003) Multiple actions of angiotensin II in hypertension: benefits of AT1 receptor blockade. J Am Coll Cardiol 42:911-913
42. Srinivasan S, Hatley ME, Bolick DT, Palmer LA, Edelstein D, Brownlee M, Hedrick CC (2004) Hyperglycaemia-induced superoxide production decreases eNOS expression via AP-1 activation in aortic endothelial cells. Diabetologia 47:1727-1734
43. Sukumar P, Viswambharan H, Imrie H, Cubbon RM, Yuldasheva N, Gage M, Galloway S, Skromna A, Kandavelu P, Santos CX, Gatenby VK, Smith J, Beech DJ, Wheatcroft SB, Channon KM, Shah AM, Kearney MT (2013) Nox2 NADPH oxidase has a critical role in insulin resistance-related endothelial cell dysfunction. Diabetes 62:2130-2134
44. Sun Y, Zhang J, Lu L, Chen SS, Quinn MT, Weber KT (2002) Aldosterone-induced inflammation in the rat heart: role of oxidative stress. Am J Pathol 161:1773-1781
45. Tawfik HE, El-Remessy AB, Matragoon S, Ma G, Caldwell RB, Caldwell RW (2006) Simvastatin improves diabetes-induced coronary endothelial dysfunction. J Pharmacol Exp Ther 319:386-395
46. Taye A, Saad AH, Kumar AH, Morawietz H (2010) Effect of apocynin on NADPH oxidase-mediated oxidative stress-LOX-1-eNOS pathway in human endothelial cells exposed to high glucose. Eur J Pharmacol 627:42-48
47. Taye A, Abouzied MM, Mohafez OM (2013) Tempol ameliorates cardiac fibrosis in streptozotocin-induced diabetic rats: role of oxidative stress in diabetic cardiomyopathy. Naunyn Schmiedeberg's Arch Pharmacol 386:1071-1080
48. Triggle CR, Ding H (2010) A review of endothelial dysfunction in diabetes: a focus on the contribution of a dysfunctional eNOS. J Am Soc Hypertens 4:102-115
49. Tsutsui H, Matsushima S, Kinugawa S, Ide T, Inoue N, Ohta Y, Yokota T, Hamaguchi S, Sunagawa K (2007) Angiotensin II type 1 receptor blocker attenuates myocardial remodeling and preserves diastolic function in diabetic heart. Hypertens Res 30:439-449
50. Wendt MC, Daiber A, Kleschyov AL, Mülsch A, Sydow K, Schulz E, Chen K, Keaney JF Jr, Lassègue B, Walter U, Griendling KK, Münzel T (2005) Differential effects of diabetes on the expression of the gp91phox homologues nox1 and nox4. Free Radic Biol Med 39:381-391
51. Wenzel P, Schulz E, Oleze M, Müller J, Schuhmacher S, Alhamadani MS, Debrezion J, Hortmann M, Reifenberg K, Felming I, Münzel, Daiber A (2008) AT1-receptor blockade by telmisartan upregulates GTP-cyclohydrolase I and protects eNOS in diabetic rats. Free Radic Biol Med 45:619-626
52. Wong WT, Tian XY, Xu A, Ng CF, Lee HK, Chen ZY, Au CL, Yao X, Huang Y (2010) Angiotensin II type 1 receptor-dependent oxidative stress mediates endothelial dysfunction in type 2 diabetic mice. Antioxid Redox Signal 13:757-768
53. Zayachkivska O, Gzregotsky M, Ferentc M, Yaschenko A, Urbanovych A (2008) Effects of nitrosative stress and reactive oxygen-scavenging systems in esophageal physiopathy under streptozotocin-induced experimental hyperglycemia. J Physiol Pharmacol 59(Suppl 2):77-87