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Published in: Urolithiasis 6/2016

01-11-2016 | Original Paper

Hyperoxaluria-induced tubular ischemia: the effects of verapamil on the antioxidant capacity of the affected kidneys

Authors: Kemal Sarica, Alper Kafkasli, Fehmi Narter, Oguz Ozturk, Ozgur Yazici, Bilal Hamarat, Cahit Sahin, Bilal Eryildirim

Published in: Urolithiasis | Issue 6/2016

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Abstract

To evaluate the potential protective effects of a calcium channel blocker (Verapamil) on the oxidative stress related changes with an emphasis on the antioxidant capacity of the kidneys an experimental study in rats was performed. A total of 44 rats have been included. Hyperoxaluria was induced in Group 1 by continuous administration of ethylene glycol (EG). Animals in Group 2 received Verapamil in addition to EG. Animals in Group 3 constituted the control group. In addition to the evaluation of tissue and serum levels of three scavenging enzymes, NO, MDA and T-AOC; the presence and degree of crystal formation in renal parenchyma were evaluated in all animals after 7 and 28 days. Our data demonstrated that in addition to the lower level of all three scavenging enzymes (SOD, CAT and GSH) particularly during late phase evaluation (4 weeks); the total antioxidant capacity (T-AOC) of these kidneys were also higher when compared with the animals receiving EG only. Tissue and serum levels of both NO and MDA indicated the preventive effect of Verapamil on the oxidative stress induced changes. Very limited or no crystallization in the kidneys treated with verapamil during early and late phase examination was observed when compared with considerable crystal formation in Group 2 animals. Verapamil treatment may preserve the oxidant capacity of the kidneys and subsequently limit the crystal deposition induced by hyperoxaluria. Verapamil could therefore be considered in the management of kidney stone formation particularly in cases with recurrent kidney stone disease.
Literature
2.
go back to reference Hackett RL, Shevock PN, Khan SR (1994) Madin-Darby canine kidney cells are injured by exposure to oxalate and to calcium oxalate crystals. Urol Res 22:197CrossRefPubMed Hackett RL, Shevock PN, Khan SR (1994) Madin-Darby canine kidney cells are injured by exposure to oxalate and to calcium oxalate crystals. Urol Res 22:197CrossRefPubMed
3.
go back to reference Thamilselvan S, Khan SR (1998) Oxalate and calcium oxalate crystals are injurious to renal epithelial cells: results of in vivo and in vitro studies. J Nephrol 11:66PubMed Thamilselvan S, Khan SR (1998) Oxalate and calcium oxalate crystals are injurious to renal epithelial cells: results of in vivo and in vitro studies. J Nephrol 11:66PubMed
4.
go back to reference Khan SR (1995) Calcium oxalate crystal interaction with renal tubular epithelium, mechanism of crystal adhesion and its impact on stone development. Urol Res 23:71CrossRefPubMed Khan SR (1995) Calcium oxalate crystal interaction with renal tubular epithelium, mechanism of crystal adhesion and its impact on stone development. Urol Res 23:71CrossRefPubMed
5.
go back to reference Khaskhali MH, Byer KJ, Khan SR (2009) The effect of calcium on calcium oxalate monohydrate crystal induced renal epithelial injury. Urol Res 37(1):1–6CrossRefPubMed Khaskhali MH, Byer KJ, Khan SR (2009) The effect of calcium on calcium oxalate monohydrate crystal induced renal epithelial injury. Urol Res 37(1):1–6CrossRefPubMed
6.
go back to reference Koul H, Kennington L, Honeyman T et al (1996) Activation of c-myc gene mediates the mitogenic effects of oxalate in LLC-PK1 cells, a line of renal epithelial cells. Kidney Int 50:1525–1530CrossRefPubMed Koul H, Kennington L, Honeyman T et al (1996) Activation of c-myc gene mediates the mitogenic effects of oxalate in LLC-PK1 cells, a line of renal epithelial cells. Kidney Int 50:1525–1530CrossRefPubMed
7.
go back to reference Scheid C, Koul H, Hill WA et al (1996) Oxalate toxicity in LLC-PK1 cells, a line of renal epithelial cells. J Urol 155:1112–1116CrossRefPubMed Scheid C, Koul H, Hill WA et al (1996) Oxalate toxicity in LLC-PK1 cells, a line of renal epithelial cells. J Urol 155:1112–1116CrossRefPubMed
8.
go back to reference Sarica K, Yagcı F, Bakır K, Erturhan S, Ucak R (2001) Renal tubular injury induced by hyperoxaluria: evaluation of apoptotic changes. Urol Res 29:34CrossRefPubMed Sarica K, Yagcı F, Bakır K, Erturhan S, Ucak R (2001) Renal tubular injury induced by hyperoxaluria: evaluation of apoptotic changes. Urol Res 29:34CrossRefPubMed
9.
go back to reference Hackett RL, Shevock PN, Khan SR (1995) Alterations in MDCK and LLC-PK1 cells exposed to oxalate and calcium oxalate monohydrate crystals. Scanning Micorosc 9:587 Hackett RL, Shevock PN, Khan SR (1995) Alterations in MDCK and LLC-PK1 cells exposed to oxalate and calcium oxalate monohydrate crystals. Scanning Micorosc 9:587
10.
go back to reference Davalos M, Konno S, Eshghi M, Choudhury M (2010) Oxidative renal cell injury induced by calcium oxalate crystal and reno protection with antioxidants: a possible role of oxidative stress in nephrolithiasis. J Endourol 24(3):339–345CrossRefPubMed Davalos M, Konno S, Eshghi M, Choudhury M (2010) Oxidative renal cell injury induced by calcium oxalate crystal and reno protection with antioxidants: a possible role of oxidative stress in nephrolithiasis. J Endourol 24(3):339–345CrossRefPubMed
11.
go back to reference Khan SR (2004) Crystal-induced inflammation of the kidneys: results from human studies, animal models and tissue-culture studies. Clin Exp Nephrol 8:75–88CrossRefPubMed Khan SR (2004) Crystal-induced inflammation of the kidneys: results from human studies, animal models and tissue-culture studies. Clin Exp Nephrol 8:75–88CrossRefPubMed
12.
go back to reference Khan SR (2006) Renal tubular damage/dysfunction: key to the formation of kidney stones. Urol Res 34:86–91CrossRefPubMed Khan SR (2006) Renal tubular damage/dysfunction: key to the formation of kidney stones. Urol Res 34:86–91CrossRefPubMed
13.
go back to reference Thamilselvan S, Khan SR, Menon M (2003) Oxalate and calcium oxalate mediated free radical toxicity in renal epithelial cells: effect of antioxidants. Urol Res 31:3–9PubMed Thamilselvan S, Khan SR, Menon M (2003) Oxalate and calcium oxalate mediated free radical toxicity in renal epithelial cells: effect of antioxidants. Urol Res 31:3–9PubMed
14.
go back to reference Bhandari A, Koul S, Sekhon A et al (2002) Effects of oxalate on HK-2 cells, a line of proximal tubular epithelial cells from normal human kidney. J Urol 168:253–259CrossRefPubMed Bhandari A, Koul S, Sekhon A et al (2002) Effects of oxalate on HK-2 cells, a line of proximal tubular epithelial cells from normal human kidney. J Urol 168:253–259CrossRefPubMed
15.
go back to reference Khan SR (2014) Reactive oxygen species, inflammation and calcium oxalate nephrolithiasis. Transl Androl Urol 3(3):256–276PubMedPubMedCentral Khan SR (2014) Reactive oxygen species, inflammation and calcium oxalate nephrolithiasis. Transl Androl Urol 3(3):256–276PubMedPubMedCentral
16.
17.
go back to reference Silva JP, Coutinho OP (2010) Free radicals in the regulation of damage and cell death – basicmechanisms and prevention. Drug Discov Ther 4(3):144–167PubMed Silva JP, Coutinho OP (2010) Free radicals in the regulation of damage and cell death – basicmechanisms and prevention. Drug Discov Ther 4(3):144–167PubMed
18.
go back to reference Wilcox JK, Ash SL, Catignani GL (2004) Antioxidants and prevention of chronic disease. Crit Rev Food Sci Nutr 44:275–295CrossRef Wilcox JK, Ash SL, Catignani GL (2004) Antioxidants and prevention of chronic disease. Crit Rev Food Sci Nutr 44:275–295CrossRef
19.
go back to reference Halliwell B, Aeschbach R, Loliger J, Aruoma OI (1995) The characterization of antioxidants. Food Chem Toxicol 33:601–617CrossRefPubMed Halliwell B, Aeschbach R, Loliger J, Aruoma OI (1995) The characterization of antioxidants. Food Chem Toxicol 33:601–617CrossRefPubMed
20.
go back to reference Biri H, Ozturk HS, Buyukkocak S, Kacmaz M (1998) Antioxidant defense potential of rabbit renal tissues after ESWL: protective effect of antioxidant vitamins. Nephron 79:181CrossRefPubMed Biri H, Ozturk HS, Buyukkocak S, Kacmaz M (1998) Antioxidant defense potential of rabbit renal tissues after ESWL: protective effect of antioxidant vitamins. Nephron 79:181CrossRefPubMed
21.
go back to reference Thamilselvan S, Byer KJ, Hackett RL, Khan SR (2000) Free radical scavengers, catalase and superoxide dismutase provide protection from oxalate associated injury to LLC-PK1 and MDCK cells. J Urol 164:224–229CrossRefPubMed Thamilselvan S, Byer KJ, Hackett RL, Khan SR (2000) Free radical scavengers, catalase and superoxide dismutase provide protection from oxalate associated injury to LLC-PK1 and MDCK cells. J Urol 164:224–229CrossRefPubMed
22.
go back to reference Park HK, Jeong BC, Sung MK et al (2008) Reduction of oxidative stress in cultured renal tubular cells and preventive effects on renal stone formation by the bioflavonoid quercetin. J Urol 179(4):1620–1626CrossRefPubMed Park HK, Jeong BC, Sung MK et al (2008) Reduction of oxidative stress in cultured renal tubular cells and preventive effects on renal stone formation by the bioflavonoid quercetin. J Urol 179(4):1620–1626CrossRefPubMed
23.
go back to reference Khan SR, Shevock PN, Hackett RL (1993) Magnesium oxide administration and prevention of calcium oxalate nephrolithiasis. J Urol 149:412PubMed Khan SR, Shevock PN, Hackett RL (1993) Magnesium oxide administration and prevention of calcium oxalate nephrolithiasis. J Urol 149:412PubMed
24.
go back to reference Sahin C, Sarikaya S, Sarica K et al (2015) Limitation of apoptotic changes and crystal deposition by Tutukon following hyperoxaluria-induced tubular cell injury in rat model. Urolithiasis 43(4):313–322CrossRefPubMed Sahin C, Sarikaya S, Sarica K et al (2015) Limitation of apoptotic changes and crystal deposition by Tutukon following hyperoxaluria-induced tubular cell injury in rat model. Urolithiasis 43(4):313–322CrossRefPubMed
25.
go back to reference Tanriverdi O, Telci D, Aydin M, Ekici ID, Miroglu C, Sarıca K (2012) Hyperoxaluria-induced tubular ischemia: the effects of verapamil and vitamin E on apoptotic changes with an emphasis on renal papilla in rat model. Urol Res 40(1):17–25CrossRefPubMed Tanriverdi O, Telci D, Aydin M, Ekici ID, Miroglu C, Sarıca K (2012) Hyperoxaluria-induced tubular ischemia: the effects of verapamil and vitamin E on apoptotic changes with an emphasis on renal papilla in rat model. Urol Res 40(1):17–25CrossRefPubMed
26.
go back to reference Benyi L, Weilherg Z, Puyun L (1995) Protective effects of nifedipine and allopurinol on high energy shock wave induced acute changes of renal function. J Urol 153:596CrossRef Benyi L, Weilherg Z, Puyun L (1995) Protective effects of nifedipine and allopurinol on high energy shock wave induced acute changes of renal function. J Urol 153:596CrossRef
27.
go back to reference Sarica K, Bakır K, Yagcı F, Topcu O, Akbay C, Sayın N, Korkmaz C (1999) Limitation of possible enhanced crystal deposition by verapamil in renal parenchyma after shock wave application in rabbit model. J Endourol 13:343CrossRefPubMed Sarica K, Bakır K, Yagcı F, Topcu O, Akbay C, Sayın N, Korkmaz C (1999) Limitation of possible enhanced crystal deposition by verapamil in renal parenchyma after shock wave application in rabbit model. J Endourol 13:343CrossRefPubMed
28.
go back to reference Strohmaier WL, Abelius A, Billes J, Grossmann T, Wilbert DM, Bichler KH (1994) Verapamil limits shock wave-induced renal tubular damage in vivo. J Endourol 8:269CrossRefPubMed Strohmaier WL, Abelius A, Billes J, Grossmann T, Wilbert DM, Bichler KH (1994) Verapamil limits shock wave-induced renal tubular damage in vivo. J Endourol 8:269CrossRefPubMed
29.
go back to reference Yencilek F, Sarica K, Eryildirim B, Erturhan S, Karakok M, Kuyumcuoglu U (2010) Hyperoxaluria-induced tubular ischemia: the effect of verapamil on the limitation of tissue HIF-1 alpha levels in renal parenchyma. Int Urol Nephrol 42(2):361–367CrossRefPubMed Yencilek F, Sarica K, Eryildirim B, Erturhan S, Karakok M, Kuyumcuoglu U (2010) Hyperoxaluria-induced tubular ischemia: the effect of verapamil on the limitation of tissue HIF-1 alpha levels in renal parenchyma. Int Urol Nephrol 42(2):361–367CrossRefPubMed
30.
go back to reference Sarica K, Erturhan S, Altay B (2007) Effect of verapamil on urinary stone-forming risk factors. Urol Res 35(1):23–27CrossRefPubMed Sarica K, Erturhan S, Altay B (2007) Effect of verapamil on urinary stone-forming risk factors. Urol Res 35(1):23–27CrossRefPubMed
31.
go back to reference Byer K, Khan SR (2005) Citrate provides protection against oxalate and calcium oxalate crystal induced oxidative damage to renal epithelium. J Urol 173(2):640–646CrossRefPubMed Byer K, Khan SR (2005) Citrate provides protection against oxalate and calcium oxalate crystal induced oxidative damage to renal epithelium. J Urol 173(2):640–646CrossRefPubMed
32.
go back to reference Tracy CR, Pearle MS (2009) Update on the medical management of stone disease. Curr Opin Urol 19(2):200–204CrossRefPubMed Tracy CR, Pearle MS (2009) Update on the medical management of stone disease. Curr Opin Urol 19(2):200–204CrossRefPubMed
33.
go back to reference Huang HS, Chen J, Chen CF et al (2006) Vitamin E attenuates crystal formation in rat kidneys: roles of renal tubular cell death and crystallization inhibitors. Kidney Int 70:699–710CrossRefPubMed Huang HS, Chen J, Chen CF et al (2006) Vitamin E attenuates crystal formation in rat kidneys: roles of renal tubular cell death and crystallization inhibitors. Kidney Int 70:699–710CrossRefPubMed
34.
go back to reference Huang HS, Chen J, Chen CF, Ma MC (2006) Vitamin E attenuates crystal formation in rat kidneys: roles of renal tubular cell death and crystallization inhibitors. Kidney Int 70(4):699–710 (erratum (2007) 71(7):712) Huang HS, Chen J, Chen CF, Ma MC (2006) Vitamin E attenuates crystal formation in rat kidneys: roles of renal tubular cell death and crystallization inhibitors. Kidney Int 70(4):699–710 (erratum (2007) 71(7):712)
35.
go back to reference Thamilselvan S, Hackett RL, Khan SR (1997) Lipid peroxidation in ethylene glycol induced hyperoxaluria and calcium Oxalate nephrolithiasis. J Urol 157:1059–1063CrossRefPubMed Thamilselvan S, Hackett RL, Khan SR (1997) Lipid peroxidation in ethylene glycol induced hyperoxaluria and calcium Oxalate nephrolithiasis. J Urol 157:1059–1063CrossRefPubMed
36.
go back to reference Muhtukumar A, Selvam R (1997) Renal injury mediated calcium oxalate nephrolithiasis: role of lipid peroxidation. Ren Fail 19:401–408CrossRef Muhtukumar A, Selvam R (1997) Renal injury mediated calcium oxalate nephrolithiasis: role of lipid peroxidation. Ren Fail 19:401–408CrossRef
37.
go back to reference Huang HS, Ma MC, Chen CF et al (2003) Lipid peroxidation and its correlations with urinary levels of oxalate, citric acid, and osteopontin in patients with renal calcium oxalate stones. Urology 62:1123–1128CrossRefPubMed Huang HS, Ma MC, Chen CF et al (2003) Lipid peroxidation and its correlations with urinary levels of oxalate, citric acid, and osteopontin in patients with renal calcium oxalate stones. Urology 62:1123–1128CrossRefPubMed
38.
go back to reference Strohmaier WL, Bichler KH, Koch J, Balk KN, Wilbert DM (1993) Protective effect of verapamil on shock wave-induced renal tubular dysfunction. J Urol 150:27PubMed Strohmaier WL, Bichler KH, Koch J, Balk KN, Wilbert DM (1993) Protective effect of verapamil on shock wave-induced renal tubular dysfunction. J Urol 150:27PubMed
39.
go back to reference Huang HS, Ma MC, Chen J et al (2002) Changes in the oxidant antioxidant balance in the kidney of rats with nephrolithiasis induced by ethylene glycol. J Urol 167:2584–2593CrossRefPubMed Huang HS, Ma MC, Chen J et al (2002) Changes in the oxidant antioxidant balance in the kidney of rats with nephrolithiasis induced by ethylene glycol. J Urol 167:2584–2593CrossRefPubMed
40.
go back to reference Dobashi K, Ghosh B, Orak JK, Singh I, Singh AK (2000) Kidney ischemia-reperfusion: modulation of antioxidant defenses. Mol Cell Biochem 205(1–2):1–11CrossRefPubMed Dobashi K, Ghosh B, Orak JK, Singh I, Singh AK (2000) Kidney ischemia-reperfusion: modulation of antioxidant defenses. Mol Cell Biochem 205(1–2):1–11CrossRefPubMed
41.
go back to reference Baggio B, Gambaro G, Ossi E et al (1983) Increased urinary excretion of renal enzymes in idiopathic calcium oxalate nephrolithiasis. J Urol 129:1161–1162PubMed Baggio B, Gambaro G, Ossi E et al (1983) Increased urinary excretion of renal enzymes in idiopathic calcium oxalate nephrolithiasis. J Urol 129:1161–1162PubMed
42.
go back to reference Boonla C, Wunsuwan R, Tungsanga K et al (2007) Urinary 8-hydroxy-deoxyguanosine is elevated in patients with nephrolithiasis. Urol Res 35:185–191CrossRefPubMed Boonla C, Wunsuwan R, Tungsanga K et al (2007) Urinary 8-hydroxy-deoxyguanosine is elevated in patients with nephrolithiasis. Urol Res 35:185–191CrossRefPubMed
43.
go back to reference Thamilselvan S, Byer KJ, Hackett RL et al (2000) Free radical scavengers, catalase and superoxide dismutase provide protection from oxalate-associated injury to LLC-PK1 and MDCK cells. J Urol 164:224–229CrossRefPubMed Thamilselvan S, Byer KJ, Hackett RL et al (2000) Free radical scavengers, catalase and superoxide dismutase provide protection from oxalate-associated injury to LLC-PK1 and MDCK cells. J Urol 164:224–229CrossRefPubMed
44.
go back to reference Gáspár S, Niculiţe C, Cucu D et al (2010) Effect of calcium oxalate on renal cells as revealed by real-time measurement of extracellular oxidative burst. Biosens Bioelectron 25:1729–1734CrossRefPubMed Gáspár S, Niculiţe C, Cucu D et al (2010) Effect of calcium oxalate on renal cells as revealed by real-time measurement of extracellular oxidative burst. Biosens Bioelectron 25:1729–1734CrossRefPubMed
45.
go back to reference Messiha BA, Abo-Youssef AM (2015) Protective effects of fish oil, allopurinol, and verapamil on hepatic ischemia-reperfusion injury in rats. J Nat Sci Biol Med. Jul-Dec 6(2):351–355CrossRef Messiha BA, Abo-Youssef AM (2015) Protective effects of fish oil, allopurinol, and verapamil on hepatic ischemia-reperfusion injury in rats. J Nat Sci Biol Med. Jul-Dec 6(2):351–355CrossRef
46.
go back to reference Zhang J, Cao H, Zhang Y, Zhang Y et al (2013) Nephroprotective effect of calcium channel blockers against toxicity of lead exposure in mice. Toxicol Lett 218(3):273–280 Zhang J, Cao H, Zhang Y, Zhang Y et al (2013) Nephroprotective effect of calcium channel blockers against toxicity of lead exposure in mice. Toxicol Lett 218(3):273–280
47.
go back to reference Bhattacharya SK, Rathi N, Mahajan P et al (2009) Effect of Ocimum sanctum, ascorbic acid, and verapamil on macrophage function and oxidative stress in mice exposed to cocaine. Indian J Pharmacol 41(3):134–9 Bhattacharya SK, Rathi N, Mahajan P et al (2009) Effect of Ocimum sanctum, ascorbic acid, and verapamil on macrophage function and oxidative stress in mice exposed to cocaine. Indian J Pharmacol 41(3):134–9
48.
go back to reference Miller NJ, Rice-Evans C, Davies MJ, Gopinathan V, Milner A (1993) A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clin Sci 84:407–412CrossRefPubMed Miller NJ, Rice-Evans C, Davies MJ, Gopinathan V, Milner A (1993) A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clin Sci 84:407–412CrossRefPubMed
49.
go back to reference Kusano C, Ferrari B (2008) Total antioxidant capacity: a biomarker in biomedical and nutritional studies. J. Cel. Mol. Biol. 7(1):1–15 Kusano C, Ferrari B (2008) Total antioxidant capacity: a biomarker in biomedical and nutritional studies. J. Cel. Mol. Biol. 7(1):1–15
50.
go back to reference Iguchi M, Ikegami M, Kiwamoto H et al (1993) Effect of verapamil on urinary calcium and oxalate excretion in renal stone formers. Hinyokika Kiyo 39(5):425–431PubMed Iguchi M, Ikegami M, Kiwamoto H et al (1993) Effect of verapamil on urinary calcium and oxalate excretion in renal stone formers. Hinyokika Kiyo 39(5):425–431PubMed
51.
go back to reference Jan CR, Chen WC, Wu SN et al (1998) Nifedipine, verapamil and diltiazem block shock-wave-induced rises in cytosolic calcium in MDCK cells. Chin J Physiol 41(4):181–188PubMed Jan CR, Chen WC, Wu SN et al (1998) Nifedipine, verapamil and diltiazem block shock-wave-induced rises in cytosolic calcium in MDCK cells. Chin J Physiol 41(4):181–188PubMed
52.
go back to reference Tanaka T, Nangaku M, Miyata T et al (2004) Blockade of calcium influx through L-type calcium channels attenuates mitochondrial injury and apoptosis in hypoxic renal tubular cells. J Am Soc Nephrol 15(9):2320–2333CrossRefPubMed Tanaka T, Nangaku M, Miyata T et al (2004) Blockade of calcium influx through L-type calcium channels attenuates mitochondrial injury and apoptosis in hypoxic renal tubular cells. J Am Soc Nephrol 15(9):2320–2333CrossRefPubMed
53.
go back to reference Ogawa Y, Hayashi K, Nakahama T et al (2001) Role of T-type calcium channels in renal microcirculation: studies in the isolated perfused hydronephrotic kidney. Hypertension 38:343–347CrossRef Ogawa Y, Hayashi K, Nakahama T et al (2001) Role of T-type calcium channels in renal microcirculation: studies in the isolated perfused hydronephrotic kidney. Hypertension 38:343–347CrossRef
54.
go back to reference Epstein M (2002) Calcium antagonists in the mamagement of hypertension. Calcium antagonists in clinical medicine. Hanley and Belfus, Philadelphia, pp 293–313 Epstein M (2002) Calcium antagonists in the mamagement of hypertension. Calcium antagonists in clinical medicine. Hanley and Belfus, Philadelphia, pp 293–313
55.
go back to reference Goaling P (1986) Analytical reviews in clinical biochemistry: calcium measurement. Ann Clin Bichem 23:146CrossRef Goaling P (1986) Analytical reviews in clinical biochemistry: calcium measurement. Ann Clin Bichem 23:146CrossRef
56.
go back to reference Krieg M, Gunsser KJ, Steinhagen-Tessen E, Becker H (1986) Comparative quantitative clinico-chemical analyses of the characteristics of 24-hour urine and morning urine. J Clin Chem Clin Biochem 24:863PubMed Krieg M, Gunsser KJ, Steinhagen-Tessen E, Becker H (1986) Comparative quantitative clinico-chemical analyses of the characteristics of 24-hour urine and morning urine. J Clin Chem Clin Biochem 24:863PubMed
57.
go back to reference Frishman WH (1994) Current status of calcium channel blockers. Curr Probl Cardiol 19:637–688 (50) Frishman WH (1994) Current status of calcium channel blockers. Curr Probl Cardiol 19:637–688 (50)
58.
go back to reference Carmines PK, Fowler BC, Bell PD (1993) Segmentally distinct effects of depolarization on intracellular [Ca2+] in renal arterioles. Am J Physiol 265(5 Pt 2):677–685 Carmines PK, Fowler BC, Bell PD (1993) Segmentally distinct effects of depolarization on intracellular [Ca2+] in renal arterioles. Am J Physiol 265(5 Pt 2):677–685
59.
go back to reference Hayashi K, Nagahama T, Oka K, Epstein M, Saruta T (1996) Disparate effects of calcium antagonists on renal microcirculation. Hypertens Res 19(1):31–36CrossRefPubMed Hayashi K, Nagahama T, Oka K, Epstein M, Saruta T (1996) Disparate effects of calcium antagonists on renal microcirculation. Hypertens Res 19(1):31–36CrossRefPubMed
60.
go back to reference Grossman E, Messerli FH (1998) Effect of calcium antagonists on sympathetic activity. Eur Heart J 19(Suppl F):F27–F31PubMed Grossman E, Messerli FH (1998) Effect of calcium antagonists on sympathetic activity. Eur Heart J 19(Suppl F):F27–F31PubMed
61.
go back to reference Mason RP, Marche P, Hintze TH (2003) Novel vascular biology of third-generation L-type calcium channel antagonists: ancillary actions of amlodipine. Arterioscler Thromb Vasc Biol 23(12):2155–2163CrossRefPubMed Mason RP, Marche P, Hintze TH (2003) Novel vascular biology of third-generation L-type calcium channel antagonists: ancillary actions of amlodipine. Arterioscler Thromb Vasc Biol 23(12):2155–2163CrossRefPubMed
62.
go back to reference Epstein M (1992) Calcium antagonists and renal protection: current status and future perspectives. Arch Intern Med 152:1573–1584CrossRefPubMed Epstein M (1992) Calcium antagonists and renal protection: current status and future perspectives. Arch Intern Med 152:1573–1584CrossRefPubMed
63.
go back to reference Epstein M (2002) Calcium antagonists and the kidney: implications for renal protection. Calcium antagonists in clinical medicine. Hanley and Belfus, Philadelphia, pp 629–664 Epstein M (2002) Calcium antagonists and the kidney: implications for renal protection. Calcium antagonists in clinical medicine. Hanley and Belfus, Philadelphia, pp 629–664
64.
go back to reference Epstein M (2002) Calcium antagonists in the management of hypertension. In: Calcium antagonists in clinical medicine. Hanley and Belfus, Philadelphia, pp 293–313 Epstein M (2002) Calcium antagonists in the management of hypertension. In: Calcium antagonists in clinical medicine. Hanley and Belfus, Philadelphia, pp 293–313
65.
66.
go back to reference Danon A, Zenser TV, Thomasson DL et al (1990) Effect of verapamil on prostaglandin 2 synthesis by hydronephrotic rabbit cortical interstitial cells in primary culture. J Pharmacol Exp Ther 238:125–130 Danon A, Zenser TV, Thomasson DL et al (1990) Effect of verapamil on prostaglandin 2 synthesis by hydronephrotic rabbit cortical interstitial cells in primary culture. J Pharmacol Exp Ther 238:125–130
67.
go back to reference Iguchi M, Ikegami M, Kiwamoto H et al (1993) Effect of verapamil on urinary calcium and oxalate excretion in renal stone formers. 39(5):425–431 Iguchi M, Ikegami M, Kiwamoto H et al (1993) Effect of verapamil on urinary calcium and oxalate excretion in renal stone formers. 39(5):425–431
Metadata
Title
Hyperoxaluria-induced tubular ischemia: the effects of verapamil on the antioxidant capacity of the affected kidneys
Authors
Kemal Sarica
Alper Kafkasli
Fehmi Narter
Oguz Ozturk
Ozgur Yazici
Bilal Hamarat
Cahit Sahin
Bilal Eryildirim
Publication date
01-11-2016
Publisher
Springer Berlin Heidelberg
Published in
Urolithiasis / Issue 6/2016
Print ISSN: 2194-7228
Electronic ISSN: 2194-7236
DOI
https://doi.org/10.1007/s00240-016-0894-5

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