Tempol, a superoxide dismutase-mimetic drug, prevents chronic ischemic renal injury in two-kidney, one-clip hypertensive rats

References

• Camelli S, Bobrie G, Postel-Vinay N, Azizi M, Plouin PF, Amar L. LB01.11: prevalence of secondary hypertension in young hypertensive adults. J Hypertens. 2015;33(Suppl 1):e47.
   PubMedGoogle Scholar
• Smith A, Gaba RC, Bui JT, Minocha J. Management of renovascular hypertension. Tech Vasc Interv Radiol. 2016;19:211–17.
   PubMed Web of Science ®Google Scholar
• Campos RR, Oliveira-Sales EB, Nishi EE, Boim MA, Dolnikoff MS, Bergamaschi CT. The role of oxidative stress in renovascular hypertension. Clin Exp Pharmacol Physiol. 2011;38:144–52.
   PubMed Web of Science ®Google Scholar
• Sadjadi J, Puttaparthi K, Welborn MB, Rogers TE, Moe O, Clagett GP, Turnage RH, Levi M, Modrall JG. Upregulation of autocrine-paracrine renin-angiotensin systems in chronic renovascular hypertension. J Vasc Surg. 2002;36:386–92.
   PubMed Web of Science ®Google Scholar
• Campos RR. Oxidative stress in the brain and arterial hypertension. Hypertens Res Off J Jpn Soc Hypertens. 2009;32:1047–48.
   PubMed Web of Science ®Google Scholar
• Goldblatt H, Lynch J, Hanzal RF, Summerville WW. Studies on experimental hypertension : I. The production of persistent elevation of systolic blood pressure by means of renal ischemia. J Exp Med. 1934;59:347–79.
   PubMedGoogle Scholar
• Navar LG, Ichihara A, Chin SY, Imig JD. Nitric oxide-angiotensin II interactions in angiotensin II-dependent hypertension. Acta Physiol Scand. 2000;168:139–47.
   PubMedGoogle Scholar
• Pradhan N, Rossi NF. Interactions between the sympathetic nervous system and angiotensin system in renovascular hypertension. Curr Hypertens Rev. 2013;9:121–29.
   PubMedGoogle Scholar
• Navar LG, Zou L, Von Thun A, Tarng Wang C, Imig JD, Mitchell KD. Unraveling the mystery of goldblatt hypertension. News Physiol Sci Int J Physiol Prod Jointly Int Union Physiol Sci Am Physiol Soc. 1998;13:170–76.
   Google Scholar
• Zimmerman MC, Lazartigues E, Sharma RV, Davisson RL. Hypertension caused by angiotensin II infusion involves increased superoxide production in the central nervous system. Circ Res. 2004;95:210–16.
   PubMed Web of Science ®Google Scholar
• Berry C, Hamilton CA, Brosnan MJ, Magill FG, Berg GA, McMurray JJ, Dominiczak AF. Investigation into the sources of superoxide in human blood vessels: angiotensin II increases superoxide production in human internal mammary arteries. Circulation. 2000;101:2206–12.
   PubMed Web of Science ®Google Scholar
• Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res. 1994;74:1141–48.
   PubMed Web of Science ®Google Scholar
• Cao Y-J, He X, Wang N, He L-C. Effects of imperatorin, the active component from Radix Angelicae (Baizhi), on the blood pressure and oxidative stress in 2K,1C hypertensive rats. Phytomedicine Int J Phytother Phytopharm. 2013;20:1048–54.
   PubMed Web of Science ®Google Scholar
• Gill PS, Wilcox CS. NADPH oxidases in the kidney. Antioxid Redox Signal. 2006;8:1597–607.
   PubMed Web of Science ®Google Scholar
• Savoia C, Burger D, Nishigaki N, Montezano A, Touyz RM. Angiotensin II and the vascular phenotype in hypertension. Expert Rev Mol Med. 2011;13:e11.
   PubMed Web of Science ®Google Scholar
• Alam MA, Chowdhury MRH, Jain P, Sagor MAT, Reza HM. DPP-4 inhibitor sitagliptin prevents inflammation and oxidative stress of heart and kidney in two kidney and one clip (2K1C) rats. Diabetol Metab Syndr. 2015;7:107.
   PubMed Web of Science ®Google Scholar
• Welch WJ, Mendonca M, Aslam S, Wilcox CS. Roles of oxidative stress and AT1 receptors in renal hemodynamics and oxygenation in the postclipped 2K,1C kidney. Hypertens Dallas Tex 1979. 2003;41:692–96.
   Google Scholar
• Son D, Kojima I, Inagi R, Matsumoto M, Fujita T, Nangaku M. Chronic hypoxia aggravates renal injury via suppression of Cu/Zn-SOD: a proteomic analysis. Am J Physiol Renal Physiol. 2008;294:F62–72.
   PubMed Web of Science ®Google Scholar
• Huang -L-L, Pan C, Yu -T-T, Guo K, Wang X-H, Zhang J-Y, Wang H-Z GS. Benefical therapeutic effect of Chinese Herbal Xinji’erkang formula on hypertension-induced renal injury in the 2-kidney-1-clip hypertensive rats. Afr J Tradit Complement Altern Med AJTCAM. 2014;11:16–27.
   PubMedGoogle Scholar
• Palm F, Onozato M, Welch WJ, Wilcox CS. Blood pressure, blood flow, and oxygenation in the clipped kidney of chronic 2-kidney, 1-clip rats: effects of tempol and Angiotensin blockade. Hypertens Dallas Tex 1979. 2010;55:298–304.
   Google Scholar
• Guron GS, Grimberg ES, Basu S, Herlitz H. Acute effects of the superoxide dismutase mimetic tempol on split kidney function in two-kidney one-clip hypertensive rats. J Hypertens. 2006;24:387–94.
   PubMed Web of Science ®Google Scholar
• Mitchell JB, Samuni A, Krishna MC, DeGraff WG, Ahn MS, Samuni U, Russo A. Biologically active metal-independent superoxide dismutase mimics. Biochemistry (Mosc). 1990;29:2802–07.
   Google Scholar
• Wilcox CS. Effects of tempol and redox-cycling nitroxides in models of oxidative stress. Pharmacol Ther. 2010;126:119–45.
   PubMed Web of Science ®Google Scholar
• Karanovic D, Grujic-Milanovic J, Miloradovic Z, Ivanov M, Jovovic D, Vajic U-J, Zivotic M, Markovic-Lipkovski J, Mihailovic-Stanojevic N. Effects of single and combined losartan and tempol treatments on oxidative stress, kidney structure and function in spontaneously hypertensive rats with early course of proteinuric nephropathy. PloS One. 2016;11:e0161706.
   PubMed Web of Science ®Google Scholar
• Costa CA, Amaral TAS, Carvalho LCRM, Ognibene DT, da Silva AFE, Moss MB, Valença SS, de Moura RS, Resende AC. Antioxidant treatment with tempol and apocynin prevents endothelial dysfunction and development of renovascular hypertension. Am J Hypertens. 2009;22:1242–49.
   PubMed Web of Science ®Google Scholar
• Xu H, Bian X, Watts SW, Hlavacova A. Activation of vascular BK channel by tempol in DOCA-salt hypertensive rats. Hypertens Dallas Tex 1979. 2005;46:1154–62.
   Google Scholar
• Wj W, Mendonca M, Blau J, Karber A, Dennehy K, Patel K, Lao Y-S, José PA, Wilcox CS. Antihypertensive response to prolonged tempol in the spontaneously hypertensive rat. Kidney Int. 2005;68:179–87.
   PubMed Web of Science ®Google Scholar
• Meng S, Cason GW, Gannon AW, Racusen LC, Manning RD. Oxidative stress in Dahl salt-sensitive hypertension. Hypertens Dallas Tex 1979. 2003;41:1346–52.
   Google Scholar
• Hoffmann DS, Weydert CJ, Lazartigues E, Kutschke WJ, Kienzle MF, Leach JE, Sharma JA, Sharma RV, Davisson RL. Chronic tempol prevents hypertension, proteinuria, and poor feto-placental outcomes in BPH/5 mouse model of preeclampsia. Hypertens Dallas Tex 1979. 2008;51:1058–65.
   Google Scholar
• Rauckman EJ, Rosen GM, Abou-donia MB. Improved methods for the oxidation of secondary amines to nitroxides. Synth Commun. 1975;5:409–13.
   Web of Science ®Google Scholar
• Souza DA, Moreno Y, Ponzio EA, Resende JALC, Jordão AK, Cunha AC, Ferreira VF, Novak MA, Vaz MGF. Synthesis, crystal structure, magnetism and electrochemical properties of two copper(II) furoyltrifluoroacetonate complexes with nitroxide radical. Inorganica Chim Acta. 2011;370:469–73.
   Web of Science ®Google Scholar
• Mcgregor DD. The effect of sympathetic nerve stimulation of vasoconstrictor responses in perfused mesenteric blood vessels of the rat. J Physiol. 1965;177:21–30.
   PubMed Web of Science ®Google Scholar
• Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–54.
   PubMed Web of Science ®Google Scholar
• Mandarim-de-Lacerda CA. Stereological tools in biomedical research. An Acad Bras Cienc. 2003;75:469–86.
   PubMed Web of Science ®Google Scholar
• Bertram JF, Soosaipillai MC, Ricardo SD, Ryan GB. Total numbers of glomeruli and individual glomerular cell types in the normal rat kidney. Cell Tissue Res. 1992;270:37–45.
   PubMed Web of Science ®Google Scholar
• Simonsen U, Christensen FH, Buus NH. The effect of tempol on endothelium-dependent vasodilatation and blood pressure. Pharmacol Ther. 2009;122:109–24.
   PubMed Web of Science ®Google Scholar
• Xu H, Jackson WF, Fink GD, Galligan JJ. Activation of potassium channels by tempol in arterial smooth muscle cells from normotensive and deoxycorticosterone acetate-salt hypertensive rats. Hypertens Dallas Tex 1979. 2006;48:1080–87.
   Google Scholar
• Lerman LO, Textor SC, Grande JP. Mechanisms of tissue injury in renal artery stenosis: ischemia and beyond. Prog Cardiovasc Dis. 2009;52:196–203.
   PubMed Web of Science ®Google Scholar
• de Oliveira-Sales EB, Nishi EE, Boim MA, Dolnikoff MS, Bergamaschi CT, Campos RR. Upregulation of AT1R and iNOS in the rostral ventrolateral medulla (RVLM) is essential for the sympathetic hyperactivity and hypertension in the 2K-1C Wistar rat model. Am J Hypertens. 2010;23:708–15.
   PubMed Web of Science ®Google Scholar
• Oliveira-Sales EB, Toward MA, Campos RR, Paton JFR. Revealing the role of the autonomic nervous system in the development and maintenance of Goldblatt hypertension in rats. Auton Neurosci Basic Clin. 2014;183:23–29.
   PubMed Web of Science ®Google Scholar
• Nishi EE, Bergamaschi CT, Campos RR. The crosstalk between the kidney and the central nervous system: the role of renal nerves in blood pressure regulation. Exp Physiol. 2015;100:479–84.
   PubMed Web of Science ®Google Scholar
• Kim YG, Lee SH, Kim S-Y, Lee A, Moon JY, Jeong K-H, Lee TW, Lim SJ, Sohn IS, Ihm C-G. Sequential activation of the intrarenal renin-angiotensin system in the progression of hypertensive nephropathy in Goldblatt rats. Am J Physiol Renal Physiol. 2016;311:F195–206.
   PubMed Web of Science ®Google Scholar
• Han Y, Fan Z-D, Yuan N, Xie G-Q, Gao J, De W, Gao X-Y, Zhu G-Q. Superoxide anions in the paraventricular nucleus mediate the enhanced cardiac sympathetic afferent reflex and sympathetic activity in renovascular hypertensive rats. J Appl Physiol Bethesda Md. 1985;2011(110):646–52.
   Google Scholar
• Oliveira-Sales EB, Dugaich AP, Carillo BA, Abreu NP, Boim MA, Martins PJ, D’Almeida V, Dolnikoff MS, Bergamaschi CT, Campos RR. Oxidative stress contributes to renovascular hypertension. Am J Hypertens. 2008;21:98–104.
   PubMed Web of Science ®Google Scholar
• Ren Y, Carretero OA, Garvin JL. Mechanism by which superoxide potentiates tubuloglomerular feedback. Hypertens Dallas Tex 1979. 2002;39:624–28.
   Google Scholar
• da Costa CA, de Oliveira PRB, de Bem GF, de Cavalho LCRM, Ognibene DT, da Silva AFE, Dos Santos Valença S, Pires KMP, da Cunha Sousa PJ, de Moura RS, et al. Euterpe oleracea Mart.-derived polyphenols prevent endothelial dysfunction and vascular structural changes in renovascular hypertensive rats: role of oxidative stress. Naunyn Schmiedebergs Arch Pharmacol. 2012;385:1199–209.
   PubMed Web of Science ®Google Scholar
• Wenzel UO, Wolf G, Jacob I, Schwegler C, Qasqas A, Amann K, Helmchen U, Stahl RAK. Beneficial and adverse renal and vascular effects of the vasopeptidase inhibitor omapatrilat in renovascular hypertensive rats. Nephrol Dial Transplant Off Publ Eur Dial Transpl Assoc - Eur Ren Assoc. 2003;18:2005–13.
   PubMed Web of Science ®Google Scholar