From the Division of Nephrology and Hypertension, Georgetown University
Medical Center, Washington, DC.
Correspondence to Christine G. Schnackenberg, PhD, Division of Nephrology and Hypertension, Georgetown University Medical Center, Building D, Room 385, 4000 Reservoir Rd NW, Washington, DC 20007.
Abstract—Superoxide radical
(O2-) is increased in the vessel wall of
spontaneously hypertensive rats (SHR) where its blockade potentiates
endothelium-dependent vasodilation. The purpose of this
study was to determine the role of O2- in the
hypertension and renal vasoconstriction of SHR and its interaction with
nitric oxide (NO). Baseline mean arterial pressure (MAP)
and renal vascular resistance were markedly elevated in SHR (n=6)
compared with Wistar-Kyoto rats (WKY; n=6) (145±4 versus 118±4
mm Hg, P<0.05, and 24±3 versus 17±1 mm Hg
· mL-1 · min-1, respectively;
P<0.05). The stable membrane-permeable superoxide
dismutase mimetic 4-hydroxy-2,2,6,6-tetramethyl piperidine-1-oxyl
(tempol; 72 µmol/kg IV) normalized MAP (103±9 versus 96±6
mm Hg for SHR and WKY, respectively) and RVR (17±2 versus 15±1
mm Hg · mL-1 · min-1) of SHR.
The MAP of SHR was more sensitive and responsive to graded infusions of
tempol (0, 1.8, 18, 180, and 1800 µmol ·
kg-1 · h-1 IV) than that of WKY. To
determine whether O2- increases MAP by
inactivation of NO, its synthesis was blocked in SHR with
Nw-nitro-L-arginine methyl ester
(L-NAME, 11 µmol · kg-1 ·
min-1 IV, n=6). Whereas tempol alone significantly reduced
MAP by 32% (184±12 to 121±18 mm Hg, P<0.05,
n=6), L-NAME infusion abolished the MAP response to tempol (187±8 to
186±4 mm Hg, n=5). In contrast, tempol did reduce MAP of SHR
(188±7 to 161±7 mm Hg, P<0.05) where MAP was
elevated by norepinephrine (31 nmol ·
kg-1 · min-1 IV, n=6). Finally, to
determine the longer-term effect of O2-,
tempol (1.5 mmol · kg-1 ·
d-1 IP) was given for 7 days. Tempol had no effect on MAP
in WKY (96±1 to 97±1 mm Hg, n=7) but significantly decreased
MAP in SHR (133±2 to 120±3 mm Hg, P<0.05, n=7).
These data implicate O2- in the hypertension
of SHR in vivo. The antihypertensive action of tempol depends on NO
synthesis presumably because O2-
inactivates NO and thus diminishes its vasodilatory
actions.
© 1998 American Heart Association, Inc.
Scientific Contributions
Normalization of Blood Pressure and Renal Vascular Resistance in SHR With a Membrane-Permeable Superoxide Dismutase Mimetic
Role of Nitric Oxide
Key Words: free radicals • superoxide dismutase • nitric oxide • antioxidants • tempol • blood pressure
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A. D. Dobrian, S. D. Schriver, T. Lynch, and R. L. Prewitt Effect of salt on hypertension and oxidative stress in a rat model of diet-induced obesity Am J Physiol Renal Physiol, October 1, 2003; 285(4): F619 - F628. [Abstract] [Full Text] [PDF]
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G. E. Callera, R. M. Touyz, S. A. Teixeira, M. N. Muscara, M. H. C. Carvalho, Z. B. Fortes, D. Nigro, E. L. Schiffrin, and R. C. Tostes ETA Receptor Blockade Decreases Vascular Superoxide Generation in DOCA-Salt Hypertension Hypertension, October 1, 2003; 42(4): 811 - 817. [Abstract] [Full Text] [PDF]
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L. Li, S. W. Watts, A. K. Banes, J. J. Galligan, G. D. Fink, and A. F. Chen NADPH Oxidase-Derived Superoxide Augments Endothelin-1-Induced Venoconstriction in Mineralocorticoid Hypertension Hypertension, September 1, 2003; 42(3): 316 - 321. [Abstract] [Full Text] [PDF]
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A. Makino, M. M. Skelton, A.-P. Zou, and A. W. Cowley Jr Increased Renal Medullary H2O2 Leads to Hypertension Hypertension, July 1, 2003; 42(1): 25 - 30. [Abstract] [Full Text] [PDF]
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Q. Pu, M. F. Neves, A. Virdis, R. M. Touyz, and E. L. Schiffrin Endothelin Antagonism on Aldosterone-Induced Oxidative Stress and Vascular Remodeling Hypertension, July 1, 2003; 42(1): 49 - 55. [Abstract] [Full Text] [PDF]
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S. Meng, G. W. Cason, A. W. Gannon, L. C. Racusen, and R. D. Manning Jr Oxidative Stress in Dahl Salt-Sensitive Hypertension Hypertension, June 1, 2003; 41(6): 1346 - 1352. [Abstract] [Full Text] [PDF]
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J. F. Reckelhoff and J. C. Romero Role of oxidative stress in angiotensin-induced hypertension Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2003; 284(4): R893 - R912. [Abstract] [Full Text] [PDF]
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Y. Chu, S. Iida, D. D. Lund, R. M. Weiss, G. F. DiBona, Y. Watanabe, F. M. Faraci, and D. D. Heistad Gene Transfer of Extracellular Superoxide Dismutase Reduces Arterial Pressure in Spontaneously Hypertensive Rats: Role of Heparin-Binding Domain Circ. Res., March 7, 2003; 92(4): 461 - 468. [Abstract] [Full Text] [PDF]
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K. M. Hoagland, K. G. Maier, and R. J. Roman Contributions of 20-HETE to the Antihypertensive Effects of Tempol in Dahl Salt-Sensitive Rats Hypertension, March 1, 2003; 41(3): 697 - 702. [Abstract] [Full Text] [PDF]
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L. Li, G. D. Fink, S. W. Watts, C. A. Northcott, J. J. Galligan, P. J. Pagano, and A. F. Chen Endothelin-1 Increases Vascular Superoxide via EndothelinA-NADPH Oxidase Pathway in Low-Renin Hypertension Circulation, February 25, 2003; 107(7): 1053 - 1058. [Abstract] [Full Text] [PDF]
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T. L. Pallone, Z. Zhang, and K. Rhinehart Physiology of the renal medullary microcirculation Am J Physiol Renal Physiol, February 1, 2003; 284(2): F253 - F266. [Abstract] [Full Text] [PDF]
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T. Shokoji, A. Nishiyama, Y. Fujisawa, H. Hitomi, H. Kiyomoto, N. Takahashi, S. Kimura, M. Kohno, and Y. Abe Renal Sympathetic Nerve Responses to Tempol in Spontaneously Hypertensive Rats Hypertension, February 1, 2003; 41(2): 266 - 273. [Abstract] [Full Text] [PDF]
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B. Rodriguez-Iturbe, C.-D. Zhan, Y. Quiroz, R. K. Sindhu, and N. D. Vaziri Antioxidant-Rich Diet Relieves Hypertension and Reduces Renal Immune Infiltration in Spontaneously Hypertensive Rats Hypertension, February 1, 2003; 41(2): 341 - 346. [Abstract] [Full Text] [PDF]
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N. Kawada, E. Imai, A. Karber, W. J. Welch, and C. S. Wilcox A Mouse Model of Angiotensin II Slow Pressor Response: Role of Oxidative Stress J. Am. Soc. Nephrol., December 1, 2002; 13(12): 2860 - 2868. [Abstract] [Full Text] [PDF]
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F. Krotz, H. Y. Sohn, M. Keller, T. Gloe, S. S. Bolz, B. F. Becker, and U. Pohl Depolarization of Endothelial Cells Enhances Platelet Aggregation Through Oxidative Inactivation of Endothelial NTPDase Arterioscler. Thromb. Vasc. Biol., December 1, 2002; 22(12): 2003 - 2009. [Abstract] [Full Text] [PDF]
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C. A. Hamilton, M. J. Brosnan, S. Al-Benna, G. Berg, and A. F. Dominiczak NAD(P)H Oxidase Inhibition Improves Endothelial Function in Rat and Human Blood Vessels Hypertension, November 1, 2002; 40(5): 755 - 762. [Abstract] [Full Text] [PDF]
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H. Xu, G. D. Fink, and J. J. Galligan Nitric oxide-independent effects of tempol on sympathetic nerve activity and blood pressure in DOCA-salt rats Am J Physiol Heart Circ Physiol, September 1, 2002; 283(3): H885 - H892. [Abstract] [Full Text] [PDF]
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S. Adler and H. Huang Impaired Regulation of Renal Oxygen Consumption in Spontaneously Hypertensive Rats J. Am. Soc. Nephrol., July 1, 2002; 13(7): 1788 - 1794. [Abstract] [Full Text] [PDF]
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 X. J. Zhou, N. D. Vaziri, X. Q. Wang, F. G. Silva, and Z. Laszik Nitric Oxide Synthase Expression in Hypertension Induced by Inhibition of Glutathione Synthase J. Pharmacol. Exp. Ther., March 1, 2002; 300(3): 762 - 767. [Abstract] [Full Text] [PDF]
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 M. Rathaus and J. Bernheim Oxygen species in the microvascular environment: regulation of vascular tone and the development of hypertension Nephrol. Dial. Transplant., February 1, 2002; 17(2): 216 - 221. [Abstract] [Full Text] [PDF]
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C. G. Schnackenberg Physiological and pathophysiological roles of oxygen radicals in the renal microvasculature Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2002; 282(2): R335 - R342. [Abstract] [Full Text] [PDF]
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T. Chabrashvili, A. Tojo, M. L. Onozato, C. Kitiyakara, M. T. Quinn, T. Fujita, W. J. Welch, and C. S. Wilcox Expression and Cellular Localization of Classic NADPH Oxidase Subunits in the Spontaneously Hypertensive Rat Kidney Hypertension, February 1, 2002; 39(2): 269 - 274. [Abstract] [Full Text] [PDF]
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D. S.A. Majid and A. Nishiyama Nitric Oxide Blockade Enhances Renal Responses to Superoxide Dismutase Inhibition in Dogs Hypertension, February 1, 2002; 39(2): 293 - 297. [Abstract] [Full Text] [PDF]
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A. E. Midaoui and J. de Champlain Prevention of Hypertension, Insulin Resistance, and Oxidative Stress by {alpha}-Lipoic Acid Hypertension, February 1, 2002; 39(2): 303 - 307. [Abstract] [Full Text] [PDF]
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Y. Ren, O. A. Carretero, and J. L. Garvin Mechanism by Which Superoxide Potentiates Tubuloglomerular Feedback Hypertension, February 1, 2002; 39(2): 624 - 628. [Abstract] [Full Text] [PDF]
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A. Makino, M. M. Skelton, A.-P. Zou, R. J. Roman, and A. W. Cowley Jr Increased Renal Medullary Oxidative Stress Produces Hypertension Hypertension, February 1, 2002; 39(2): 667 - 672. [Abstract] [Full Text] [PDF]
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D. M. Attia, A. M. G. Verhagen, E. S. G. Stroes, E. E. van Faassen, H.-J. Grone, S. J. De Kimpe, H. A. Koomans, B. Braam, and J. A. Joles Vitamin E Alleviates Renal Injury, but Not Hypertension, during Chronic Nitric Oxide Synthase Inhibition in Rats J. Am. Soc. Nephrol., December 1, 2001; 12(12): 2585 - 2593. [Abstract] [Full Text] [PDF]
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M.-G. Feng, S. A. W. Dukacz, and R. L. Kline Selective effect of tempol on renal medullary hemodynamics in spontaneously hypertensive rats Am J Physiol Regulatory Integrative Comp Physiol, November 1, 2001; 281(5): R1420 - R1425. [Abstract] [Full Text] [PDF]
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