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Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Research Article

Combination of Captopril with Gliclazide Decreases Vascular and Renal Complications and Improves Glycemic Control in Rats with Streptozotocin- Induced Diabetes Mellitus

Author(s): Sayed M.M. Mizar*, Magy R. Kozman, Ali A. Abo-Saif and Basim A.S. Messiha

Volume 21, Issue 6, 2021

Published on: 21 August, 2020

Page: [1096 - 1106] Pages: 11

DOI: 10.2174/1871530320666200821160436

Price: $65

Abstract

Background: The common antihypertensive angiotensin-converting enzyme (ACE) inhibitor captopril was reported to possess anti-oxidant and anti-inflammatory effects in different experimental models. Diabetic vascular complications arise from increased vascular endothelial inflammation and oxidative stress as well as decreased nitric oxide bioavailability in the vessel walls due to poor glycemic control.

Objective: This study aimed to evaluate the role of captopril and gliclazide in decreasing diabetes mellitus (DM) vascular complications caused by decreased cellular glucose uptake and impaired endothelial nitric oxide metabolism, as well as examine the effects of the combination on diabetic renal complication and plasma lipid profile.

Methods: Adult male Wister rats received captopril (25 mg/kg/day) and/or gliclazide (10 mg/kg/- day) by oral gavage daily for one month after induction of DM using streptozotocin (50 mg/kg, i.p., once). Serum glucose and insulin levels, inflammatory mediators like TNF-α, oxidative stress biomarkers like glutathione and nitric oxide, and plasma lipid profile were measured. Besides, histopathological examination of the thoracic aorta and kidney tissues, Western blot assessed the expression of nitric oxide synthase (NOS) subtypes in the thoracic aorta.

Results: Captopril significantly improved vascular architecture and oxidative stress and modulated nitric oxide synthesis via regulation of nitric oxide synthases, as well as decreased inflammation via down-regulating TNF-α, decreased systolic and diastolic blood pressure, and improved serum lipid profile in diabetic rats. Gliclazide increased serum insulin and decreased serum glucose, as well as its anti-oxidant and anti-inflammatory effects.

Conclusion: Captopril showed a promising protective effect against DM vascular complications, at least via nitric oxide modulating effect, anti-oxidant effect, and anti-inflammatory activity that appeared in biochemical and histopathological findings, lipid profile, renal function, and architecture improvements. Combining gliclazide with captopril gives an additive effect through enhanced glycemic control and increased anti-oxidant and anti-inflammatory properties above captopril alone.

Keywords: Nitric oxide synthase, anti-oxidant, streptozotocin, anti-inflammatory, hyperglycemia, lipid profile, renal function.

Graphical Abstract

[1]
Akash, M.S.H.; Rehman, K.; Liaqat, A. Tumor necrosis factor‐alpha: role in development of insulin resistance and pathogenesis of type 2 diabetes mellitus. J. Cell. Biochem., 2018, 119(1), 105-110.
[http://dx.doi.org/10.1002/jcb.26174] [PMID: 28569437]
[2]
Asmat, U.; Abad, K.; Ismail, K. Diabetes mellitus and oxidative stress-A concise review. Saudi Pharm. J., 2016, 24(5), 547-553.
[http://dx.doi.org/10.1016/j.jsps.2015.03.013] [PMID: 27752226]
[3]
Tanveer, A.; Akram, K.; Farooq, U.; Hayat, Z.; Shafi, A. Management of diabetic complications through fruit flavonoids as a natural remedy. Crit. Rev. Food Sci. Nutr., 2017, 57(7), 1411-1422.
[http://dx.doi.org/10.1080/10408398.2014.1000482] [PMID: 26065867]
[4]
Aksnes, T.A.; Kjeldsen, S.E.; Rostrup, M.; Holzhauer, B.; Hua, T.A.; Julius, S. Predictors of cardiac morbidity in diabetic, new-onset diabetic and non-diabetic high-risk hypertensive patients: The Valsartan Antihypertensive Long-term Use Evaluation (VALUE) trial. Blood Press., 2016, 25(4), 235-240.
[http://dx.doi.org/10.3109/08037051.2015.1134071] [PMID: 26808585]
[5]
Domanski, M.J.; Farkouh, M.E.; Zak, V.; Feske, S.; Easton, D.; Weinberger, J.; Hamon, M.; Escobedo, J.; Shrader, P.; Siami, F.S.; Fuster, V. Predictors of stroke associated with coronary artery bypass grafting in patients with diabetes mellitus and multivessel coronary artery disease. Am. J. Cardiol., 2015, 115(10), 1382-1388.
[http://dx.doi.org/10.1016/j.amjcard.2015.02.033] [PMID: 25824543]
[6]
Dubouchaud, H.; Walter, L.; Rigoulet, M.; Batandier, C. Mitochondrial NADH redox potential impacts the reactive oxygen species production of reverse Electron transfer through complex I. J. Bioenerg. Biomembr., 2018, 50(5), 367-377.
[http://dx.doi.org/10.1007/s10863-018-9767-7] [PMID: 30136168]
[7]
Grundy, S.M. Metabolic syndrome update. Trends Cardiovasc. Med., 2016, 26(4), 364-373.
[http://dx.doi.org/10.1016/j.tcm.2015.10.004] [PMID: 26654259]
[8]
Rovira-Llopis, S.; Bañuls, C.; de Marañon, A.M.; Diaz-Morales, N.; Jover, A.; Garzon, S.; Rocha, M.; Victor, V.M.; Hernandez-Mijares, A. Low testosterone levels are related to oxidative stress, mitochondrial dysfunction and altered subclinical atherosclerotic markers in type 2 diabetic male patients. Free Radic. Biol. Med., 2017, 108, 155-162.
[http://dx.doi.org/10.1016/j.freeradbiomed.2017.03.029] [PMID: 28359952]
[9]
Kayama, Y.; Raaz, U.; Jagger, A.; Adam, M.; Schellinger, I.N.; Sakamoto, M.; Suzuki, H.; Toyama, K.; Spin, J.M.; Tsao, P.S. Diabetic cardiovascular disease induced by oxidative stress. Int. J. Mol. Sci., 2015, 16(10), 25234-25263.
[http://dx.doi.org/10.3390/ijms161025234] [PMID: 26512646]
[10]
Lind, M.; Hayes, A.; Caprnda, M.; Petrovic, D.; Rodrigo, L.; Kruzliak, P.; Zulli, A. Inducible nitric oxide synthase: Good or bad? Biomed. Pharmacother., 2017, 93, 370-375.
[http://dx.doi.org/10.1016/j.biopha.2017.06.036] [PMID: 28651238]
[11]
Greenberg, H.Z.; Shi, J.; Jahan, K.S.; Martinucci, M.C.; Gilbert, S.J.; Vanessa Ho, W.S.; Albert, A.P. Stimulation of calcium-sensing receptors induces endothelium-dependent vasorelaxations via nitric oxide production and activation of IKCa channels. Vascul. Pharmacol., 2016, 80, 75-84.
[http://dx.doi.org/10.1016/j.vph.2016.01.001] [PMID: 26772767]
[12]
Chen, Z.Q.; Mou, R.T.; Feng, D.X.; Wang, Z.; Chen, G. The role of nitric oxide in stroke. Med. Gas Res., 2017, 7(3), 194-203.
[http://dx.doi.org/10.4103/2045-9912.215750] [PMID: 29152213]
[13]
Predonzani, A.; Calì, B.; Agnellini, A.H.; Molon, B. Spotlights on immunological effects of reactive nitrogen species: When inflammation says nitric oxide. World J. Exp. Med., 2015, 5(2), 64-76.
[http://dx.doi.org/10.5493/wjem.v5.i2.64] [PMID: 25992321]
[14]
Forrester, S.J.; Kikuchi, D.S.; Hernandes, M.S.; Xu, Q.; Griendling, K.K. Reactive oxygen species in metabolic and inflammatory signaling. Circ. Res., 2018, 122(6), 877-902.
[http://dx.doi.org/10.1161/CIRCRESAHA.117.311401] [PMID: 29700084]
[15]
Quintana-Villamandos, B.; Delgado-Baeza, E. Does the ADMA/DDAH/NO pathway modulate early regression of left ventricular hypertrophy with esmolol? Med. Hypotheses, 2016, 87, 44-47.
[http://dx.doi.org/10.1016/j.mehy.2015.12.016] [PMID: 26826640]
[16]
Bernátová, I.; Pechánová, O.; Pelouch, V.; Simko, F. Regression of chronic L -NAME-treatment-induced left ventricular hypertrophy: effect of captopril. J. Mol. Cell. Cardiol., 2000, 32(2), 177-185.
[http://dx.doi.org/10.1006/jmcc.1999.1071] [PMID: 10722795]
[17]
Irondi, E.A.; Agboola, S.O.; Oboh, G.; Boligon, A.A.; Athayde, M.L.; Shode, F.O. Guava leaves polyphenolics-rich extract inhibits vital enzymes implicated in gout and hypertension in vitro. J. Intercult. Ethnopharmacol., 2016, 5(2), 122-130.
[http://dx.doi.org/10.5455/jice.20160321115402] [PMID: 27104032]
[18]
Flores-Monroy, J.; Ferrario, C.M.; Valencia-Hernández, I.; Hernández-Campos, M.E.; Martínez-Aguilar, L. Comparative effects of a novel angiotensin-converting enzyme inhibitor versus captopril on plasma angiotensins after myocardial infarction. Pharmacology, 2014, 94(1-2), 21-28.
[http://dx.doi.org/10.1159/000365093] [PMID: 25171296]
[19]
Sola, D.; Rossi, L.; Schianca, G.P.C.; Maffioli, P.; Bigliocca, M.; Mella, R.; Corlianò, F.; Fra, G.P.; Bartoli, E.; Derosa, G. Sulfonylureas and their use in clinical practice. Arch. Med. Sci., 2015, 11(4), 840-848.
[http://dx.doi.org/10.5114/aoms.2015.53304] [PMID: 26322096]
[20]
Gribble, F.M.; Reimann, F. Differential selectivity of insulin secretagogues: mechanisms, clinical implications, and drug interactions. J. Diabetes Complications, 2003, 17(2)(Suppl.), 11-15.
[http://dx.doi.org/10.1016/S1056-8727(02)00272-6] [PMID: 12623163]
[21]
Vetriselvam, V.; Rajkumar, A.; Krishnamoorthi, S. Effects of chronic antioxidant supplementation in diabetic mellitus patients. Free Radic. Biol. Med., 2018, 128, S41.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.10.061]
[22]
Fava, D.; Cassone-Faldetta, M.; Laurenti, O.; De Luca, O.; Ghiselli, A.; De Mattia, G. Gliclazide improves anti-oxidant status and nitric oxide-mediated vasodilation in Type 2 diabetes. Diabet. Med., 2002, 19(9), 752-757.
[http://dx.doi.org/10.1046/j.1464-5491.2002.00762.x] [PMID: 12207812]
[23]
Chen, L-L.; Yu, F.; Zeng, T.S.; Liao, Y.F.; Li, Y.M.; Ding, H.C. Effects of gliclazide on endothelial function in patients with newly diagnosed type 2 diabetes. Eur. J. Pharmacol., 2011, 659(2-3), 296-301.
[http://dx.doi.org/10.1016/j.ejphar.2011.02.044] [PMID: 21453695]
[24]
Pawelczyk, M.; Kaczorowska, B.; Baj, Z. The impact of hyperglycemia and hyperlipidemia on plasma P-selectin and platelet markers after ischemic stroke. Arch. Med. Sci., 2017, 13(5), 1049-1056.
[http://dx.doi.org/10.5114/aoms.2017.65816] [PMID: 28883845]
[25]
El-Marasy, S.A.; Abdallah, H.M.; El-Shenawy, S.M.; El-Khatib, A.S.; El-Shabrawy, O.A.; Kenawy, S.A. Anti-depressant effect of hesperidin in diabetic rats. Can. J. Physiol. Pharmacol., 2014, 92(11), 945-952.
[http://dx.doi.org/10.1139/cjpp-2014-0281] [PMID: 25358020]
[26]
Zhang, H.; Yang, Y.; Wang, Y.; Wang, B.; Li, R. Renal-protective effect of thalidomide in streptozotocin-induced diabetic rats through anti-inflammatory pathway. Drug Des. Devel. Ther., 2018, 12, 89-98.
[http://dx.doi.org/10.2147/DDDT.S149298] [PMID: 29386886]
[27]
Park, H-S.; Han, A.; Yeo, H-L.; Park, M.J.; You, M.J.; Choi, H.J.; Hong, C.W.; Lee, S.H.; Kim, S.H.; Kim, B.; Kwon, M.S. Chronic high dose of captopril induces depressive-like behaviors in mice: possible mechanism of regulatory T cell in depression. Oncotarget, 2017, 8(42), 72528-72543.
[http://dx.doi.org/10.18632/oncotarget.19879] [PMID: 29069807]
[28]
Jeenger, M.K.; Shrivastava, S.; Yerra, V.G.; Naidu, V.G.; Ramakrishna, S.; Kumar, A. Curcumin: a pleiotropic phytonutrient in diabetic complications. Nutrition, 2015, 31(2), 276-282.
[http://dx.doi.org/10.1016/j.nut.2014.06.015] [PMID: 25441584]
[29]
Furman, B.L. Streptozotocin‐induced diabetic models in mice and rats. Curr. Protocols Pharmacol., 2015, 70, 1-20, 20.
[http://dx.doi.org/10.1002/0471141755.ph0547s70] [PMID: 26331889]
[30]
Hassan, S.K.; El-Sammad, N.M.; Mousa, A.M. Hypoglycemic and antioxidant activities of Caesalpinia ferrea Martius leaf extract in streptozotocin-induced diabetic rats. Asian Pac. J. Trop. Biomed., 2015, 5, 462-471.
[http://dx.doi.org/10.1016/j.apjtb.2015.03.004]
[31]
Badawy, D.; El-Bassossy, H.M.; Fahmy, A.; Azhar, A. Aldose reductase inhibitors zopolrestat and ferulic acid alleviate hypertension associated with diabetes: effect on vascular reactivity. Can. J. Physiol. Pharmacol., 2013, 91(2), 101-107.
[http://dx.doi.org/10.1139/cjpp-2012-0232] [PMID: 23458193]
[32]
Barham, D.; Trinder, P. An improved colour reagent for the determination of blood glucose by the oxidase system. Analyst (Lond.), 1972, 97(151), 142-145.
[http://dx.doi.org/10.1039/an9729700142] [PMID: 5037807]
[33]
Grebenchtchikov, N.; Geurts-Moespot, A.J.; Kroot, J.J.; den Heijer, M.; Tjalsma, H.; Swinkels, D.W.; Sweep, F.G. High-sensitive radioimmunoassay for human serum hepcidin. Br. J. Haematol., 2009, 146(3), 317-325.
[http://dx.doi.org/10.1111/j.1365-2141.2009.07758.x] [PMID: 19500086]
[34]
Engelberts, I.; Möller, A.; Schoen, G.J.; van der Linden, C.J.; Buurman, W.A. Evaluation of measurement of human TNF in plasma by ELISA. Lymphokine Cytokine Res., 1991, 10(1-2), 69-76.
[PMID: 1873359]
[35]
Sedlak, J.; Lindsay, R.H. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal. Biochem., 1968, 25(1), 192-205.
[http://dx.doi.org/10.1016/0003-2697(68)90092-4] [PMID: 4973948]
[36]
Nims, R.W.; Darbyshire, J.F.; Saavedra, J.E. Colorimetric methods for the determination of nitric oxide concentration in neutral aqueous solutions. Methods, 1995, 7, 48-54.
[http://dx.doi.org/10.1006/meth.1995.1007]
[37]
Allain, C.C.; Poon, L.S.; Chan, C.S.; Richmond, W.; Fu, P.C. Enzymatic determination of total serum cholesterol. Clin. Chem., 1974, 20(4), 470-475.
[http://dx.doi.org/10.1093/clinchem/20.4.470] [PMID: 4818200]
[38]
Burstein, M.; Scholnick, H.R.; Morfin, R. Rapid method for the isolation of lipoproteins from human serum by precipitation with polyanions. J. Lipid Res., 1970, 11(6), 583-595.
[http://dx.doi.org/10.1016/S0022-2275(20)42943-8] [PMID: 4100998]
[39]
Friedewald, W.T.; Levy, R.I.; Fredrickson, D.S. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin. Chem., 1972, 18(6), 499-502.
[http://dx.doi.org/10.1093/clinchem/18.6.499] [PMID: 4337382]
[40]
Fossati, P.; Prencipe, L. Serum triglycerides determined colorimetrically with an enzyme that produces hydrogen peroxide. Clin. Chem., 1982, 28(10), 2077-2080.
[http://dx.doi.org/10.1093/clinchem/28.10.2077] [PMID: 6812986]
[41]
Fawcett, J.K.; Scott, J.E. A rapid and precise method for the determination of urea. J. Clin. Pathol., 1960, 13, 156-159.
[http://dx.doi.org/10.1136/jcp.13.2.156] [PMID: 13821779]
[42]
Bartels, H.; Böhmer, M.; Heierli, C. [Serum creatinine determination without protein precipitation]. Clin. Chim. Acta, 1972, 37, 193-197.
[http://dx.doi.org/10.1016/0009-8981(72)90432-9] [PMID: 5022083]
[43]
Mizar, S.M.; Omar, H.A.; El Sherbiny, G.A. Nebivolol and chrysin protect the liver against ischemia/reperfusion-induced injury in rats. Beni Suef Univ J Basic Appl Sci, 2015, 4, 86-92.
[http://dx.doi.org/10.1016/j.bjbas.2015.02.012]
[44]
Leach, J.K.; Black, S.M.; Schmidt-Ullrich, R.K.; Mikkelsen, R.B. Activation of constitutive nitric-oxide synthase activity is an early signaling event induced by ionizing radiation. J. Biol. Chem., 2002, 277(18), 15400-15406.
[http://dx.doi.org/10.1074/jbc.M110309200] [PMID: 11856735]
[45]
Ganz, T.; Wainstein, J.; Gilad, S.; Limor, R.; Boaz, M.; Stern, N. Serum asymmetric dimethylarginine and arginine levels predict microvascular and macrovascular complications in type 2 diabetes mellitus. Diabetes Metab. Res. Rev., 2017, 33(2), 2836-2844.
[http://dx.doi.org/10.1002/dmrr.2836] [PMID: 27393712]
[46]
Liu, J-J.; Foo, J.P.; Liu, S.; Lim, S.C. The role of fibroblast growth factor 21 in diabetes and its complications: A review from clinical perspective. Diabetes Res. Clin. Pract., 2015, 108(3), 382-389.
[http://dx.doi.org/10.1016/j.diabres.2015.02.032] [PMID: 25796513]
[47]
Harding, J.L.; Pavkov, M.E.; Magliano, D.J.; Shaw, J.E.; Gregg, E.W. Global trends in diabetes complications: a review of current evidence. Diabetologia, 2019, 62(1), 3-16.
[http://dx.doi.org/10.1007/s00125-018-4711-2] [PMID: 30171279]
[48]
El-Bassossy, H.M.; Hassan, N.A.; Mahmoud, M.F.; Fahmy, A. Baicalein protects against hypertension associated with diabetes: effect on vascular reactivity and stiffness. Phytomedicine, 2014, 21(12), 1742-1745.
[http://dx.doi.org/10.1016/j.phymed.2014.08.012] [PMID: 25442285]
[49]
Soleimani, A-R.; Akbari, H.; Soleimani, S.; Beladi Mousavi, S.S.; Tamadon, M.R. Effect of sour tea (Lipicom) pill versus captopril on the treatment of hypertension. J. Renal Inj. Prev., 2015, 4(3), 73-79.
[PMID: 26468478]
[50]
Dojki, F.K.; Bakris, G.L. Blood pressure control and cardiovascular/renal outcomes. Endocrinol. Metab. Clin. North Am., 2018, 47(1), 175-184.
[http://dx.doi.org/10.1016/j.ecl.2017.10.008] [PMID: 29407050]
[51]
Morris, D. Complications of diabetes: Keeping an eye on retinopathy. Independent Nurse, 2018, 5, 15-18.
[http://dx.doi.org/10.12968/indn.2018.5.15]
[52]
Khalil, H. Diabetes microvascular complications-A clinical update. Diabetes Metab. Syndr., 2017, 11(Suppl. 1), S133-S139.
[http://dx.doi.org/10.1016/j.dsx.2016.12.022] [PMID: 27993541]
[53]
Abd Allah, E.S.; Gomaa, A.M. Effects of curcumin and captopril on the functions of kidney and nerve in streptozotocin-induced diabetic rats: role of angiotensin converting enzyme 1. Appl. Physiol. Nutr. Metab., 2015, 40(10), 1061-1067.
[http://dx.doi.org/10.1139/apnm-2015-0145] [PMID: 26398443]
[54]
Goossens, G.H. The renin-angiotensin system in the pathophysiology of type 2 diabetes. Obes. Facts, 2012, 5(4), 611-624.
[http://dx.doi.org/10.1159/000342776] [PMID: 22986649]
[55]
Öztaş, E.; Yılmaz, T.E.; Güzel, E.; Sezer, Z.; Okyar, A.; Özhan, G. Gliclazide alone or in combination with atorvastatin ameliorated reproductive damage in streptozotocin-induced type 2 diabetic male rats. Saudi Pharm. J., 2019, 27(3), 422-431.
[http://dx.doi.org/10.1016/j.jsps.2019.01.003] [PMID: 30976187]
[56]
Sepehri, Z.; Masoumi, M.; Ebrahimi, N.; Kiani, Z.; Nasiri, A.A.; Kohan, F.; Sheikh Fathollahi, M.; Kazemi Arababadi, M.; Asadikaram, G. Atorvastatin, losartan and captopril lead to upregulation of TGF-β, and downregulation of IL-6 in coronary artery disease and hypertension. PLoS One, 2016, 11(12), e0168312.
[http://dx.doi.org/10.1371/journal.pone.0168312] [PMID: 28033321]
[57]
Alizadeh, S.; Mazloom, H.; Sadeghi, A.; Emamgholipour, S.; Golestani, A.; Noorbakhsh, F.; Khoshniatnikoo, M.; Meshkani, R. Evidence for the link between defective autophagy and inflammation in peripheral blood mononuclear cells of type 2 diabetic patients. J. Physiol. Biochem., 2018, 74(3), 369-379.
[http://dx.doi.org/10.1007/s13105-018-0624-2] [PMID: 29654511]
[58]
El-Ashmawy, N.E.; Khedr, N.F.; El-Bahrawy, H.A.; Hamada, O.B. Anti-inflammatory and Antioxidant Effects of Captopril Compared to Methylprednisolone in L-Arginine-Induced Acute Pancreatitis. Dig. Dis. Sci., 2018, 63(6), 1497-1505.
[http://dx.doi.org/10.1007/s10620-018-5036-1] [PMID: 29594979]
[59]
Petrov, L.; Atanassova, M.; Alexandrova, A. Comparative study of the antioxidant activity of some thiol-containing substances. Open Med., 2012, 7, 269-273.
[http://dx.doi.org/10.2478/s11536-011-0132-z]
[60]
Yaseen, R.; Pushpalatha, H.; Reddy, G.B.; Ismael, A.; Ahmed, A.; Dheyaa, A.; Ovais, S.; Rathore, P.; Samim, M.; Akthar, M.; Sharma, K.; Shafi, S.; Singh, S.; Javed, K. Design and synthesis of pyridazinone-substituted benzenesulphonylurea derivatives as anti-hyperglycaemic agents and inhibitors of aldose reductase - an enzyme embroiled in diabetic complications. J. Enzyme Inhib. Med. Chem., 2016, 31(6), 1415-1427.
[http://dx.doi.org/10.3109/14756366.2016.1142986] [PMID: 26879420]
[61]
Viberti, G.; Mogensen, C.E.; Groop, L.C.; Pauls, J.F. Effect of captopril on progression to clinical proteinuria in patients with insulin-dependent diabetes mellitus and microalbuminuria. JAMA, 1994, 271(4), 275-279.
[http://dx.doi.org/10.1001/jama.1994.03510280037029] [PMID: 8295285]
[62]
Tangvarasittichai, S. Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J. Diabetes, 2015, 6(3), 456-480.
[http://dx.doi.org/10.4239/wjd.v6.i3.456] [PMID: 25897356]
[63]
Singh, B.M.; Mehta, J.L. Interactions between the renin-angiotensin system and dyslipidemia: relevance in the therapy of hypertension and coronary heart disease. Arch. Intern. Med., 2003, 163(11), 1296-1304.
[http://dx.doi.org/10.1001/archinte.163.11.1296] [PMID: 12796065]
[64]
Emral, R.; Köseoğlulari, O.; Tonyukuk, V.; Uysal, A.R.; Kamel, N.; Corapçioğlu, D. The effect of short-term glycemic regulation with gliclazide and metformin on postprandial lipemia. Exp. Clin. Endocrinol. Diabetes, 2005, 113(2), 80-84.
[http://dx.doi.org/10.1055/s-2004-830536] [PMID: 15772898]
[65]
Elving, L.D.; Wetzels, J.F.; van Lier, H.J.; de Nobel, E.; Berden, J.H. Captopril and atenolol are equally effective in retarding progression of diabetic nephropathy. Results of a 2-year prospective, randomized study. Diabetologia, 1994, 37(6), 604-609.
[http://dx.doi.org/10.1007/BF00403380] [PMID: 7926346]
[66]
Yao, Y.; Davis, G.; Harrison, J.C.; Walker, R.J.; Sammut, I.A. Renal functional responses in diabetic nephropathy following chronic bilateral renal denervation. Auton. Neurosci., 2017, 204, 98-104.
[http://dx.doi.org/10.1016/j.autneu.2016.09.019] [PMID: 27727024]
[67]
van den Born, B-J.; Amraoui, F. Macrovascular Involvement in Diabetes: Renal Artery Stenosis.Diabetic Nephropathy; Springer, 2019, pp. 337-355.
[68]
McFarlane, P.; Cherney, D.; Gilbert, R.E.; Senior, P. Chronic kidney disease in diabetes. Can. J. Diabetes, 2018, 42(Suppl. 1), S201-S209.
[http://dx.doi.org/10.1016/j.jcjd.2017.11.004] [PMID: 29650098]
[69]
Saad, A.; Wang, W.; Herrmann, S.M.; Glockner, J.F.; Mckusick, M.A.; Misra, S.; Bjarnason, H.; Lerman, L.O.; Textor, S.C. Atherosclerotic renal artery stenosis is associated with elevated cell cycle arrest markers related to reduced renal blood flow and postcontrast hypoxia. Nephrol. Dial. Transplant., 2016, 31(11), 1855-1863.
[http://dx.doi.org/10.1093/ndt/gfw265] [PMID: 27474749]
[70]
Oliveira-Paula, G.H.; Pinheiro, L.C.; Ferreira, G.C.; Garcia, W.N.P.; Lacchini, R.; Garcia, L.V.; Tanus-Santos, J.E. Angiotensin converting enzyme inhibitors enhance the hypotensive effects of propofol by increasing nitric oxide production. Free Radic. Biol. Med., 2018, 115, 10-17.
[http://dx.doi.org/10.1016/j.freeradbiomed.2017.11.010] [PMID: 29138017]
[71]
Rask-Madsen, C.; King, G.L. Mechanisms of Disease: endothelial dysfunction in insulin resistance and diabetes. Nat. Clin. Pract. Endocrinol. Metab., 2007, 3(1), 46-56.
[http://dx.doi.org/10.1038/ncpendmet0366] [PMID: 17179929]

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