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(Hypertension. 1999;33:424-428.)
© 1999 American Heart Association, Inc.
Scientific Contributions |
Two-Week Administration of Tempol Attenuates Both Hypertension and Renal Excretion of 8-Iso Prostaglandin F2
From the Division of Nephrology and Hypertension, Georgetown University Medical Center, Washington, DC.
Correspondence to Christine G. Schnackenberg, PhD, Georgetown University Medical Center, Division of Nephrology and Hypertension, Bldg D, Room 385, 4000 Reservoir Rd NW, Washington, DC 20007.
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Abstract |
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Abstract—8-Iso prostaglandin F2
(8-ISO) is formed
nonenzymatically from the attack of superoxide radical on
arachidonic acid. Therefore, 8-ISO is a marker of
oxidative stress in vivo. We have recently shown that short-term
administration of the membrane-permeable, metal-independent superoxide
dismutase mimetic tempol (4-hydroxy-2, 2, 6, 6-tetramethyl
piperidinoxyl) normalizes blood pressure in spontaneously
hypertensive rats (SHR). The present study was designed to test
whether prolonged administration of tempol ameliorates oxidative stress
and hypertension in SHR. In control SHR (n=8), mean
arterial pressure and heart rate were increased and renal
blood flow and glomerular filtration rate were reduced
compared with control Wistar-Kyoto rats (WKY) (n=7). Twenty-four-hour
renal excretion of 8-ISO was significantly increased in SHR compared
with WKY. Two weeks of tempol administration in the drinking water
(1 mmol/L) to SHR (n=8) decreased mean arterial
pressure by 18% (162±8 to 134±6 mm Hg,
P<0.05), increased glomerular filtration
rate by 17% (1.6±0.2 to 1.9±0.3 mL/min), and decreased renal
excretion of 8-ISO by 39% (9.8±0.7 to 6.0±0.7 ng/24 hours,
P<0.05). In contrast, tempol administration to WKY
(n=6) had no significant effect on mean arterial pressure
(115±5 versus 118±8 mm Hg), glomerular filtration
rate (3.0±0.4 versus 2.5±0.5 mL/min), or renal excretion of 8-ISO
(7.9±0.4 versus 6.8±0.7 ng/24 hours). In conclusion, the SHR is a
model of hypertension and renal vasoconstriction associated with
oxidative stress. Because long-term administration of a superoxide
scavenger reduces blood pressure and oxidative stress in vivo, this
study suggests a role for oxygen radicals in the maintenance of
hypertension in SHR.
Key Words: oxidative stress • isoprostanes • oxygen radicals • superoxide dismutase
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Introduction |
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Reactive oxygen species (ROS) such as superoxide anion, hydroxyl radical, and hydrogen peroxide have been implicated in atherosclerosis, diabetes, ischemia/reperfusion injury, and hypertension.1 2 3 4 Compared with normotensive individuals, hypertensive patients have higher levels of plasma hydrogen peroxide, superoxide anion, and lipid peroxides, while having lower plasma levels of the antioxidant ascorbic acid.5 6 7 We8 and others9 10 11 12 have shown in short-term studies that inhibition of ROS reduces blood pressure in the spontaneously hypertensive rat (SHR). However, the importance of ROS in the long-term regulation of blood pressure in SHR has not been determined. Previous studies have shown increased superoxide release in mesenteric arterioles11 12 and cultured aortic endothelial cells,13 and increased superoxide and hydrogen peroxide release from aortic strips of SHR14 compared with the normotensive control Wistar-Kyoto rat (WKY). These studies suggest that specific vascular beds in the SHR have oxidative stress; however, it is not yet clear whether there is a net excess of ROS in SHR in vivo.
F2-isoprostanes are a family of
prostaglandin (PG) F2-like compounds
that are formed from the nonenzymatic reaction of
arachidonic acid and oxygen radicals in vivo and in
vitro.15 Because of their unique synthesis pathway,
F2-isoprostanes are recently proposed markers of
oxidative stress. For example, tissue and plasma levels of
F2-isoprostanes are increased in rats with
oxidative stress caused by carbon tetrachloride.16 Among
the several PGF2-like compounds,
8-iso-PGF2 (8-ISO) is the major urinary
metabolite of F2-isoprostanes17 and
is markedly elevated in the urine of rats after renal
ischemia/reperfusion.18
Tempol (4-hydroxy-2, 2, 6, 6-tetramethyl piperidinoxyl) is a stable, membrane-permeable, metal-independent superoxide dismutase mimetic. Tempol is a small molecular weight cyclic nitroxide that has been used as a spin trap for superoxide19 20 and reduces superoxide-related injury in ischemia/reperfusion,21 inflammation,22 and radiation.23 We have recently reported that short-term infusion or 7-day intraperitoneal administration of tempol normalizes blood pressure in the SHR.8 The aim of the present study was to assess the oxidative stress of adult SHR from the measurement of the renal excretion of 8-ISO and to determine whether long-term tempol administration ameliorates the hypertension and oxidative stress in SHR. We measured mean arterial pressure and renal hemodynamic and excretory function in WKY and SHR under normal conditions and after 2 weeks of oral tempol administration.
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Methods |
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Animal Preparation
Groups of male SHR and WKY rats (250±10 g) were maintained on tap water and a standard chow (Ralston-Purina Co, sodium content 0.3 g/100 g). Protocols were approved by the Institutional Animal Care and Use Committee of Georgetown University Medical Center and were performed according to the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health as well as the guidelines of the Animal Welfare Act. Rats were divided into four groups: WKY given vehicle (control, n=7), SHR given vehicle (control, n=8), WKY given tempol (tempol, n=6), and SHR given tempol (tempol, n=8). Tempol is readily soluble in water and was administered in the drinking water (1 mmol/L) for 2 weeks. After either control or tempol administration, rats were maintained in metabolic cages for 24 hours. Urine was collected in containers with 10 µL of 2 mmol/L EDTA to prevent ex vivo production of 8-ISO. Urine was centrifuged at 1000 rpm for 10 minutes at 4°C and stored in aliquots at -80°C until assayed.
Thereafter, WKY and SHR were anesthetized with thiobutabarbital (100 mg/kg IP, Inactin, Research Biochemicals International) and maintained at 37°C on a servo-controlled heated rodent operating table. A tracheostomy was performed with polyethylene PE-240 tubing and the left jugular vein and carotid artery were cannulated with PE-50 tubing. A 1% albumin solution in 0.154 mol/L NaCl was infused at 2 mL/h IV, to maintain a euvolemic state. A midline incision was made and the left renal artery was isolated. A blood flow probe was placed around the renal artery and connected to a transit-time blood flowmeter (1RB, Transonic Systems, Inc). We have shown previously that this method of measuring real-time changes in renal blood flow (RBF) is valid in the rat.24 Mean arterial pressure (MAP) and heart rate were recorded continuously from the carotid artery using a Statham pressure transducer (model P23, Gould Instruments) and MACLab data acquisition software. Glomerular filtration rate (GFR) was determined from the clearance of [3H]-inulin. After surgery and a 60-minute equilibration period, MAP, heart rate, GFR, and RBF were measured for 30 minutes and the data were averaged.
Determination of 8-Iso Prostaglandin F2
Urinary 8-ISO was extracted, purified, and measured according to
methods previously established using an enzyme immunoassay kit (Cayman
Chemical). Briefly, urine was spiked with
[3H]-8-ISO, treated with ethanol followed by
15% potassium hydroxide, incubated for 1 hour at 40°C, and acidified
to pH 4.0 with hydrochloric acid. The sample was extracted using a
polyboronic acid column, eluted with ethyl acetate containing 1%
methanol, and evaporated under nitrogen. 8-ISO was assayed using
competitive binding with mouse anti-rabbit IgG monoclonal antibody in a
96-well plate. Concentration of the reaction product was determined
from its absorbency at 412 nm using a standard curve. Samples were
assayed in duplicate and corrected for individual recovery of
[3H]-8-ISO. The recovery averaged 76% (n=12).
The limits of sensitivity of the assay are 1 to 3 pg/mL and the
intraassay coefficient of variation is 8% (n=6). Samples were diluted
to fall in the middle portion of the linear standard curve (10 to 100
pg/mL). To validate the collection method for measurement of 8-ISO in
urine, a second set of urine was collected from control SHR (n=5) and
WKY (n=5) in metabolic cages into containers containing 10
µL of 0.01% butylated hydroxytoluene as suggested by Roberts and
Morrow15 and assayed as described above. The results
showed a similar increase (30%) in renal excretion of 8-ISO in control
SHR compared with control WKY as described for the control groups
reported below.
Statistics
All values shown are mean ± standard error.
Analysis of variance was used to test the overall effect of
tempol. Unpaired comparisons using Student's t test were
used to determine significance between specific groups.
P<0.05 was considered statistically significant.
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Results |
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Rats maintained on tempol given in the drinking water for 2 weeks had similar dietary consumption as control rats drinking water alone. There was no significant difference between food intake (control: 25±1 versus tempol: 24±1 g/d) or body weight gain (control: 69±4 versus tempol: 66±3 g/14 days), but water intake was increased modestly in the tempol-treated groups (control: 34±2 versus tempol: 43±3 mL/day, P<0.05). Water intake was increased similarly in tempol-treated WKY and SHR.
MAP in WKY and SHR is represented in Figure 1
. Under normal conditions, MAP in SHR
was increased by 41% compared with WKY (SHR: 162±8 versus WKY:
115±5 mm Hg, P<0.001). After 2 weeks of tempol
administration, MAP was reduced in SHR to a value that was not
significantly different from WKY (SHR: 134±6 versus WKY: 118±7
mm Hg). MAP in SHR given tempol was significantly lower by 18%
compared with normal SHR. Analysis of variance showed that
tempol specifically and significantly (P<0.05) decreased
MAP in SHR. Heart rate was significantly (P<0.001) elevated
in SHR (420±6 bpm) compared with WKY (374±9 bpm) during control
conditions and was not changed by tempol (SHR: 414±9 versus WKY:
373±8 bpm).
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The Table depicts renal
hemodynamic and excretory function during control
conditions and after 2 weeks of tempol administration in the drinking
water. Under control conditions, the RBF of SHR was decreased by 34%
(SHR: 5.8±0.6 versus WKY: 8.8±0.7 mL/min, P<0.01), the
GFR was decreased by 47% (SHR: 1.6±0.2 versus WKY: 3.0±0.4 mL/min,
P<0.05), and the renal vascular resistance was
increased by 117% (SHR: 29.4±2.7 versus WKY: 13.5±1.0
mm Hg · mL-1 ·
min-1, P<0.001). After 2 weeks of
tempol administration there were no significant changes in renal
hemodynamics in SHR, although there were tendencies
toward a fall in renal vascular resistance (16%) and a rise in GFR
(17%), such that there was no longer a significant difference in GFR
between SHR and WKY. Tempol had no marked effects on renal
hemodynamics in WKY. Renal excretory function was not
significantly different between WKY and SHR during control conditions
or tempol administration. In rats of similar weight and age, we find
that urinary excretion of creatinine is 8.3±0.4 mg/24
hours in control WKY (n=6) and 7.7±0.6 mg/24 hours
creatinine in control SHR (n=6).
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Figure 2 illustrates the renal excretion
of 8-ISO in WKY and SHR. In control rats, renal excretion of 8-ISO was
elevated by 24% in SHR compared with WKY (9.8±0.7 versus 7.9±0.4
ng/24 hours, P<0.05). After 2 weeks of tempol
administration in the drinking water of SHR, the renal excretion of
8-ISO was significantly (P<0.05) reduced by 39% (6.0±0.7
ng/24 hours). However, renal excretion of 8-ISO was not significantly
affected in WKY rats given tempol in the drinking water (6.8±0.7 ng/24
hours). There was no significant difference in renal excretion of 8-ISO
between WKY and SHR after 2 weeks of tempol administration.
Analysis of variance showed that tempol specifically and
significantly (P<0.01) decreased renal excretion of 8-ISO
in SHR.
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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ROS are oxygen-containing molecules with an unpaired electron, such as superoxide, hydrogen peroxide, and hydroxyl radical, and can modulate vascular tone.25 Superoxide is a relatively abundant ROS that is dismutated enzymatically by superoxide dismutase to hydrogen peroxide. Hydrogen peroxide can be metabolized to water and oxygen by catalase or to hydroxyl radical by metal cations such as copper and iron.25 ROS are generated by normal respiration of cells and by xanthine oxidase, NADPH oxidase, glucose oxidase, cyclooxygenase,26 and nitric oxide synthase,27 28 all of which are found in the vasculature. If not kept in balance by naturally occurring enzymes such as superoxide dismutase and catalase, ROS can oxidize and destroy proteins, membrane lipids, and nucleic acids,26 diminish the biological half-life of nitric oxide,29 and generate new vasoconstrictors such as 8-ISO.15
One of the stable products when ROS attack lipids is 8-ISO. 8-ISO is generated from arachidonic acid in phospholipids and subsequently released in free form.15 Investigators have shown that 8-ISO is formed both in vitro30 and in vivo.31 Because 8-ISO is a direct, enzyme-independent, stable product of ROS, measurement of 8-ISO has been used as a marker of oxidative stress in vivo.15 Elevated renal excretion of 8-ISO has been reported in humans with scleroderma15 and preeclamptic toxemia of pregnancy32 and in rats with cyclosporin-induced nephrotoxicity,33 rhabdomyolysis,34 bile duct ligation,35 and renal ischemia/reperfusion injury.18
Measurement of the rate of excretion of 8-ISO for assessing total endogenous 8-ISO is advantageous over measurement of plasma 8-ISO for two reasons. First, this eliminates the problem of ex vivo generation of 8-ISO because the amount of lipid in urine is negligible. Second, 24-hour urinary measurement of 8-ISO presumably provides an integrated assessment of 8-ISO production with time.
The rate of excretion of 8-ISO in conscious WKY was similar to that previously reported for conscious Sprague Dawley rats.35 The finding that the SHR has an elevated rate of renal excretion of 8-ISO indicates that it is a model of oxidative stress in vivo. Prolonged tempol administration reduced renal excretion of 8-ISO significantly, consistent with reports that antioxidant therapy in rat models of oxidative stress associated with cyclosporin nephrotoxicity33 and bile duct ligation35 reduces renal excretion of 8-ISO. In the present study, the marked decrease in renal excretion of 8-ISO could not be attributed to a decrease in renal function because tempol had no significant effect on either renal hemodynamic or excretory function. In fact, 2-week tempol administration tended to improve GFR in SHR.
Previous in vivo and in vitro studies suggest that systemic vessels of SHR have increased oxidative stress, although the source of ROS remains unclear. The only previous in vivo studies in SHR show that mesenteric vessels generate oxygen radicals11 12 through xanthine oxidase.11 Earlier studies established that glomeruli generate hydrogen peroxide under normal conditions36 and can upregulate the activities of superoxide dismutase and catalase during oxidative stress.37 Overproduction of an ROS or dysregulation of antioxidants in glomeruli, other vascular beds, or tissues of SHR could contribute to the oxidative stress in this hypertensive model. We and others have shown that renal nitric oxide synthase (NOS) gene and protein expression is higher in SHR compared with WKY,38 39 but that nitric oxide generation in blood vessels is limited, perhaps because of a deficiency in the NOS cofactor tetrahydrobiopterin. Tetrahydrobiopterin deficiency enhances the formation of superoxide from NOS.27 28 In fact, addition of tetrahydrobiopterin or superoxide dismutase to the isolated aorta of SHR simultaneously reduces superoxide and increases nitric oxide production.14 These data suggest that NOS may be an important source of ROS in SHR.
Finally, 8-ISO is not only a marker of oxidative stress in vivo, but is also a vasoconstrictor. Receptors for 8-ISO have been located in rat aortic smooth muscle cells,40 retinal vascular smooth muscle cells,41 and renal arterial smooth muscle cells.18 Intrarenal infusion of 8-ISO reduces GFR and RBF in rats, in part, through activation of thromboxane A2 receptors.18 Whether elevated levels of 8-ISO in the SHR contribute to the hypertension and renal vasoconstriction remains to be determined fully. The present data show, however, that 2 weeks of antioxidant treatment with tempol decreased renal excretion of 8-ISO and blood pressure significantly but did not improve renal hemodynamics significantly, suggesting that 8-ISO may not be the primary mediator of the hypertension and renal vasoconstriction in SHR.
In conclusion, this study provides evidence that the SHR is a model of oxidative stress in vivo. The finding that a superoxide dismutase mimetic reduces blood pressure and oxidative stress in vivo suggests that oxygen radicals may be important in the long-term regulation of blood pressure in SHR. Although there are limitations in extrapolating data from the anesthetized state to the conscious state, this study provides a rational basis for a novel form of antihypertensive therapy based on tempol or similar agents. Such therapy may correct the complications created by hypertension associated with oxidative stress.
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Acknowledgments |
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This work was supported by National Institutes of Health grants DK36079, DK49870, and HL09845 and from the George E. Schreiner Chair of Nephrology. Dr Schnackenberg is a recipient of an NIH Individual National Research Service Award.
Received September 17, 1998; first decision October 12, 1998; accepted October 23, 1998.
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G. B. Silva and J. L. Garvin Angiotensin II-Dependent Hypertension Increases Na Transport-Related Oxygen Consumption by the Thick Ascending Limb Hypertension, December 1, 2008; 52(6): 1091 - 1098. [Abstract] [Full Text] [PDF]
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 L. J. Janssen Isoprostanes and Lung Vascular Pathology Am. J. Respir. Cell Mol. Biol., October 1, 2008; 39(4): 383 - 389. [Abstract] [Full Text] [PDF]
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 N. Nicolakakis, T. Aboulkassim, B. Ongali, C. Lecrux, P. Fernandes, P. Rosa-Neto, X.-K. Tong, and E. Hamel Complete Rescue of Cerebrovascular Function in Aged Alzheimer's Disease Transgenic Mice by Antioxidants and Pioglitazone, a Peroxisome Proliferator-Activated Receptor {gamma} Agonist J. Neurosci., September 10, 2008; 28(37): 9287 - 9296. [Abstract] [Full Text] [PDF]
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A. A. Banday and M. F. Lokhandwala Oxidative stress-induced renal angiotensin AT1 receptor upregulation causes increased stimulation of sodium transporters and hypertension Am J Physiol Renal Physiol, September 1, 2008; 295(3): F698 - F706. [Abstract] [Full Text] [PDF]
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A. Lopez-Ruiz, J. Sartori-Valinotti, L. L. Yanes, R. Iliescu, and J. F. Reckelhoff Sex differences in control of blood pressure: role of oxidative stress in hypertension in females Am J Physiol Heart Circ Physiol, August 1, 2008; 295(2): H466 - H474. [Abstract] [Full Text] [PDF]
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V. G. DeMarco, J. Habibi, A. T. Whaley-Connell, R. I. Schneider, R. L. Heller, J. P. Bosanquet, M. R. Hayden, K. Delcour, S. A. Cooper, B. T. Andresen, et al. Oxidative stress contributes to pulmonary hypertension in the transgenic (mRen2)27 rat Am J Physiol Heart Circ Physiol, June 1, 2008; 294(6): H2659 - H2668. [Abstract] [Full Text] [PDF]
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 T. Nagaoka, L. Kuo, Y. Ren, A. Yoshida, and T. W. Hein C-Reactive Protein Inhibits Endothelium-Dependent Nitric Oxide-Mediated Dilation of Retinal Arterioles via Enhanced Superoxide Production Invest. Ophthalmol. Vis. Sci., May 1, 2008; 49(5): 2053 - 2060. [Abstract] [Full Text] [PDF]
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J. M. Moreno, I. Rodriguez Gomez, R. Wangensteen, M. Alvarez-Guerra, J. d. D. Luna, J. Garcia-Estan, and F. Vargas Tempol improves renal hemodynamics and pressure natriuresis in hyperthyroid rats Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2008; 294(3): R867 - R873. [Abstract] [Full Text] [PDF]
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P. Xu, A. C. Costa-Goncalves, M. Todiras, L. A. Rabelo, W. O. Sampaio, M. M. Moura, S. Sousa Santos, F. C. Luft, M. Bader, V. Gross, et al. Endothelial Dysfunction and Elevated Blood Pressure in Mas Gene-Deleted Mice Hypertension, February 1, 2008; 51(2): 574 - 580. [Abstract] [Full Text] [PDF]
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T. Yada, H. Shimokawa, K. Morikawa, A. Takaki, Y. Shinozaki, H. Mori, M. Goto, Y. Ogasawara, and F. Kajiya Role of Cu,Zn-SOD in the synthesis of endogenous vasodilator hydrogen peroxide during reactive hyperemia in mouse mesenteric microcirculation in vivo Am J Physiol Heart Circ Physiol, January 1, 2008; 294(1): H441 - H448. [Abstract] [Full Text] [PDF]
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C. M. Troncoso Brindeiro, A. Q. da Silva, K. J. Allahdadi, V. Youngblood, and N. L. Kanagy Reactive oxygen species contribute to sleep apnea-induced hypertension in rats Am J Physiol Heart Circ Physiol, November 1, 2007; 293(5): H2971 - H2976. [Abstract] [Full Text] [PDF]
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E. Silva and P. Soares-da-Silva Reactive oxygen species and the regulation of renal Na+-K+-ATPase in opossum kidney cells Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2007; 293(4): R1764 - R1770. [Abstract] [Full Text] [PDF]
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M. J. Pinho, V. Pinto, M. P. Serrao, P. A. Jose, and P. Soares-da-Silva Underexpression of the Na+-dependent neutral amino acid transporter ASCT2 in the spontaneously hypertensive rat kidney Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2007; 293(1): R538 - R547. [Abstract] [Full Text] [PDF]
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S. J. Miller, L. E. Norton, M. P. Murphy, M. C. Dalsing, and J. L. Unthank The role of the renin-angiotensin system and oxidative stress in spontaneously hypertensive rat mesenteric collateral growth impairment Am J Physiol Heart Circ Physiol, May 1, 2007; 292(5): H2523 - H2531. [Abstract] [Full Text] [PDF]
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 Y. Alvarez, J. V. Perez-Giron, R. Hernanz, A. M. Briones, A. Garcia-Redondo, A. Beltran, M. J. Alonso, and M. Salaices Losartan Reduces the Increased Participation of Cyclooxygenase-2-Derived Products in Vascular Responses of Hypertensive Rats J. Pharmacol. Exp. Ther., April 1, 2007; 321(1): 381 - 388. [Abstract] [Full Text] [PDF]
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M. R. Hayden, N. A. Chowdhury, S. A. Cooper, A. Whaley-Connell, J. Habibi, L. Witte, C. Wiedmeyer, C. M. Manrique, G. Lastra, C. Ferrario, et al. Proximal tubule microvilli remodeling and albuminuria in the Ren2 transgenic rat Am J Physiol Renal Physiol, February 1, 2007; 292(2): F861 - F867. [Abstract] [Full Text] [PDF]
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A. Just, A. J. M. Olson, C. L. Whitten, and W. J. Arendshorst Superoxide mediates acute renal vasoconstriction produced by angiotensin II and catecholamines by a mechanism independent of nitric oxide Am J Physiol Heart Circ Physiol, January 1, 2007; 292(1): H83 - H92. [Abstract] [Full Text] [PDF]
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H. Xu, W. F. Jackson, G. D. Fink, and J. J. Galligan Activation of Potassium Channels by Tempol in Arterial Smooth Muscle Cells From Normotensive and Deoxycorticosterone Acetate-Salt Hypertensive Rats Hypertension, December 1, 2006; 48(6): 1080 - 1087. [Abstract] [Full Text] [PDF]
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R. Z. Fardoun, M. Asghar, and M. Lokhandwala Role of oxidative stress in defective renal dopamine D1 receptor-G protein coupling and function in old Fischer 344 rats Am J Physiol Renal Physiol, November 1, 2006; 291(5): F945 - F951. [Abstract] [Full Text] [PDF]
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W. J. Welch, T. Chabrashvili, G. Solis, Y. Chen, P. S. Gill, S. Aslam, X. Wang, H. Ji, K. Sandberg, P. Jose, et al. Role of Extracellular Superoxide Dismutase in the Mouse Angiotensin Slow Pressor Response Hypertension, November 1, 2006; 48(5): 934 - 941. [Abstract] [Full Text] [PDF]
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 A. Laskowski, O. L. Woodman, A. H. Cao, G. R. Drummond, T. Marshall, D. M. Kaye, and R. H. Ritchie Antioxidant actions contribute to the antihypertrophic effects of atrial natriuretic peptide in neonatal rat cardiomyocytes Cardiovasc Res, October 1, 2006; 72(1): 112 - 123. [Abstract] [Full Text] [PDF]
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G. B. Silva, P. A. Ortiz, N. J. Hong, and J. L. Garvin Superoxide Stimulates NaCl Absorption in the Thick Ascending Limb Via Activation of Protein Kinase C Hypertension, September 1, 2006; 48(3): 467 - 472. [Abstract] [Full Text] [PDF]
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S. Ye, H. Zhong, and V. M. Campese Oxidative Stress Mediates the Stimulation of Sympathetic Nerve Activity in the Phenol Renal Injury Model of Hypertension Hypertension, August 1, 2006; 48(2): 309 - 315. [Abstract] [Full Text] [PDF]
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A. Marwaha and M. F. Lokhandwala Tempol reduces oxidative stress and restores renal dopamine D1-like receptor- G protein coupling and function in hyperglycemic rats Am J Physiol Renal Physiol, July 1, 2006; 291(1): F58 - F66. [Abstract] [Full Text] [PDF]
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 J. C. Sullivan, J. S. Pollock, and D. M. Pollock Superoxide-dependent hypertension in male and female endothelin B receptor-deficient rats. Experimental Biology and Medicine, June 1, 2006; 231(6): 818 - 823. [Abstract] [Full Text] [PDF]
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A. Paliege, A. Parsumathy, D. Mizel, T. Yang, J. Schnermann, and S. Bachmann Effect of apocynin treatment on renal expression of COX-2, NOS1, and renin in Wistar-Kyoto and spontaneously hypertensive rats Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2006; 290(3): R694 - R700. [Abstract] [Full Text] [PDF]
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L. Kopkan and D. S.A. Majid Enhanced Superoxide Activity Modulates Renal Function in NO-Deficient Hypertensive Rats Hypertension, March 1, 2006; 47(3): 568 - 572. [Abstract] [Full Text] [PDF]
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 F. Vargas, J. M. Moreno, I. Rodriguez-Gomez, R. Wangensteen, A. Osuna, M. Alvarez-Guerra, and J. Garcia-Estan Vascular and renal function in experimental thyroid disorders Eur. J. Endocrinol., February 1, 2006; 154(2): 197 - 212. [Abstract] [Full Text] [PDF]
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K. Patel, Y. Chen, K. Dennehy, J. Blau, S. Connors, M. Mendonca, M. Tarpey, M. Krishna, J. B. Mitchell, W. J. Welch, et al. Acute antihypertensive action of nitroxides in the spontaneously hypertensive rat Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2006; 290(1): R37 - R43. [Abstract] [Full Text] [PDF]
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Y. E. Lau, J. J. Galligan, D. L. Kreulen, and G. D. Fink Activation of ETB receptors increases superoxide levels in sympathetic ganglia in vivo Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2006; 290(1): R90 - R95. [Abstract] [Full Text] [PDF]
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L. Kopkan, A. Castillo, L. G. Navar, and D. S. A. Majid Enhanced superoxide generation modulates renal function in ANG II-induced hypertensive rats Am J Physiol Renal Physiol, January 1, 2006; 290(1): F80 - F86. [Abstract] [Full Text] [PDF]
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L. T. de Richelieu, C. M. Sorensen, N.-H. Holstein-Rathlou, and M. Salomonsson NO-independent mechanism mediates tempol-induced renal vasodilation in SHR Am J Physiol Renal Physiol, December 1, 2005; 289(6): F1227 - F1234. [Abstract] [Full Text] [PDF]
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J. M. Moreno, I. R. Gomez, R. Wangensteen, A. Osuna, P. Bueno, and F. Vargas Cardiac and renal antioxidant enzymes and effects of tempol in hyperthyroid rats Am J Physiol Endocrinol Metab, November 1, 2005; 289(5): E776 - E783. [Abstract] [Full Text] [PDF]
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H. Xu, X. Bian, S. W. Watts, and A. Hlavacova Activation of Vascular BK Channel by Tempol in DOCA-Salt Hypertensive Rats Hypertension, November 1, 2005; 46(5): 1154 - 1162. [Abstract] [Full Text] [PDF]
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 A. Dikalova, R. Clempus, B. Lassegue, G. Cheng, J. McCoy, S. Dikalov, A. S. Martin, A. Lyle, D. S. Weber, D. Weiss, et al. Nox1 Overexpression Potentiates Angiotensin II-Induced Hypertension and Vascular Smooth Muscle Hypertrophy in Transgenic Mice Circulation, October 25, 2005; 112(17): 2668 - 2676. [Abstract] [Full Text] [PDF]
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C. S. Wilcox Oxidative stress and nitric oxide deficiency in the kidney: a critical link to hypertension? Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2005; 289(4): R913 - R935. [Abstract] [Full Text] [PDF]
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 N. Kobayashi, F. A. DeLano, and G. W. Schmid-Schonbein Oxidative Stress Promotes Endothelial Cell Apoptosis and Loss of Microvessels in the Spontaneously Hypertensive Rats Arterioscler Thromb Vasc Biol, October 1, 2005; 25(10): 2114 - 2121. [Abstract] [Full Text] [PDF]
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M. E. Patterson, C. R. Mouton, J. J. Mullins, and K. D. Mitchell Interactive effects of superoxide anion and nitric oxide on blood pressure and renal hemodynamics in transgenic rats with inducible malignant hypertension Am J Physiol Renal Physiol, October 1, 2005; 289(4): F754 - F759. [Abstract] [Full Text] [PDF]
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R. J. Bolterman, M. C. Manriquez, M. C. O. Ruiz, L. A. Juncos, and J. C. Romero Effects of Captopril on the Renin Angiotensin System, Oxidative Stress, and Endothelin in Normal and Hypertensive Rats Hypertension, October 1, 2005; 46(4): 943 - 947. [Abstract] [Full Text] [PDF]
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L. Kopkan and D. S. A. Majid Superoxide Contributes to Development of Salt Sensitivity and Hypertension Induced by Nitric Oxide Deficiency Hypertension, October 1, 2005; 46(4): 1026 - 1031. [Abstract] [Full Text] [PDF]
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L. A. Fortepiani and J. F. Reckelhoff Increasing oxidative stress with molsidomine increases blood pressure in genetically hypertensive rats but not normotensive controls Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2005; 289(3): R763 - R770. [Abstract] [Full Text] [PDF]
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 A. A. Banday, A. Marwaha, L. S. Tallam, and M. F. Lokhandwala Tempol Reduces Oxidative Stress, Improves Insulin Sensitivity, Decreases Renal Dopamine D1 Receptor Hyperphosphorylation, and Restores D1 Receptor-G-Protein Coupling and Function in Obese Zucker Rats Diabetes, July 1, 2005; 54(7): 2219 - 2226. [Abstract] [Full Text] [PDF]
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M. Fujita, T. Kuwaki, K. Ando, and T. Fujita Sympatho-Inhibitory Action of Endogenous Adrenomedullin Through Inhibition of Oxidative Stress in the Brain Hypertension, June 1, 2005; 45(6): 1165 - 1172. [Abstract] [Full Text] [PDF]
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E. Qamirani, Y. Ren, L. Kuo, and T. W. Hein C-Reactive Protein Inhibits Endothelium-Dependent NO-Mediated Dilation in Coronary Arterioles by Activating p38 Kinase and NAD(P)H Oxidase Arterioscler Thromb Vasc Biol, May 1, 2005; 25(5): 995 - 1001. [Abstract] [Full Text] [PDF]
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 S. Kim-Mitsuyama, E. Yamamoto, T. Tanaka, Y. Zhan, Y. Izumi, Y. Izumiya, T. Ioroi, H. Wanibuchi, and H. Iwao Critical Role of Angiotensin II in Excess Salt-Induced Brain Oxidative Stress of Stroke-Prone Spontaneously Hypertensive Rats Stroke, May 1, 2005; 36(5): 1077 - 1082. [Abstract] [Full Text] [PDF]
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S. Racasan, B. Braam, H. A. Koomans, and J. A. Joles Programming blood pressure in adult SHR by shifting perinatal balance of NO and reactive oxygen species toward NO: the inverted Barker phenomenon Am J Physiol Renal Physiol, April 1, 2005; 288(4): F626 - F636. [Abstract] [Full Text] [PDF]
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L. L. Howard, M. E. Patterson, J. J. Mullins, and K. D. Mitchell Salt-sensitive hypertension develops after transient induction of ANG II-dependent hypertension in Cyp1a1-Ren2 transgenic rats Am J Physiol Renal Physiol, April 1, 2005; 288(4): F810 - F815. [Abstract] [Full Text] [PDF]
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S. Kinugawa, Z. Wang, P. M. Kaminski, M. S. Wolin, J. G. Edwards, G. Kaley, and T. H. Hintze Limited Exercise Capacity in Heterozygous Manganese Superoxide Dismutase Gene-Knockout Mice: Roles of Superoxide Anion and Nitric Oxide Circulation, March 29, 2005; 111(12): 1480 - 1486. [Abstract] [Full Text] [PDF]
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D. S. A. Majid, A. Nishiyama, K. E. Jackson, and A. Castillo Superoxide scavenging attenuates renal responses to ANG II during nitric oxide synthase inhibition in anesthetized dogs Am J Physiol Renal Physiol, February 1, 2005; 288(2): F412 - F419. [Abstract] [Full Text] [PDF]
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W. J. Welch, J. Blau, H. Xie, T. Chabrashvili, and C. S. Wilcox Angiotensin-induced defects in renal oxygenation: role of oxidative stress Am J Physiol Heart Circ Physiol, January 1, 2005; 288(1): H22 - H28. [Abstract] [Full Text] [PDF]
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Z. Zhang, K. Rhinehart, G. Solis, J. Pittner, W. Lee-Kwon, W. J. Welch, C. S. Wilcox, and T. L. Pallone Chronic ANG II infusion increases NO generation by rat descending vasa recta Am J Physiol Heart Circ Physiol, January 1, 2005; 288(1): H29 - H36. [Abstract] [Full Text] [PDF]
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S. Adler and H. Huang Oxidant stress in kidneys of spontaneously hypertensive rats involves both oxidase overexpression and loss of extracellular superoxide dismutase Am J Physiol Renal Physiol, November 1, 2004; 287(5): F907 - F913. [Abstract] [Full Text] [PDF]
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J. M. Williams, J. S. Pollock, and D. M. Pollock Arterial Pressure Response to the Antioxidant Tempol and ETB Receptor Blockade in Rats on a High-Salt Diet Hypertension, November 1, 2004; 44(5): 770 - 775. [Abstract] [Full Text] [PDF]
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N. Kawada, K. Dennehy, G. Solis, P. Modlinger, R. Hamel, J. T. Kawada, S. Aslam, T. Moriyama, E. Imai, W. J. Welch, et al. TP receptors regulate renal hemodynamics during angiotensin II slow pressor response Am J Physiol Renal Physiol, October 1, 2004; 287(4): F753 - F759. [Abstract] [Full Text] [PDF]
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V. M. Campese, S. Ye, H. Zhong, V. Yanamadala, Z. Ye, and J. Chiu Reactive oxygen species stimulate central and peripheral sympathetic nervous system activity Am J Physiol Heart Circ Physiol, August 1, 2004; 287(2): H695 - H703. [Abstract] [Full Text] [PDF]
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T. Shokoji, Y. Fujisawa, S. Kimura, M. Rahman, H. Kiyomoto, K. Matsubara, K. Moriwaki, Y. Aki, A. Miyatake, M. Kohno, et al. Effects of Local Administrations of Tempol and Diethyldithio-Carbamic on Peripheral Nerve Activity Hypertension, August 1, 2004; 44(2): 236 - 243. [Abstract] [Full Text] [PDF]
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D. S. A. Majid, A. Nishiyama, K. E. Jackson, and A. Castillo Inhibition of nitric oxide synthase enhances superoxide activity in canine kidney Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2004; 287(1): R27 - R32. [Abstract] [Full Text] [PDF]
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T. Kishi, Y. Hirooka, Y. Kimura, K. Ito, H. Shimokawa, and A. Takeshita Increased Reactive Oxygen Species in Rostral Ventrolateral Medulla Contribute to Neural Mechanisms of Hypertension in Stroke-Prone Spontaneously Hypertensive Rats Circulation, May 18, 2004; 109(19): 2357 - 2362. [Abstract] [Full Text] [PDF]
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B. Rodriguez-Iturbe, N. D. Vaziri, J. Herrera-Acosta, and R. J. Johnson Oxidative stress, renal infiltration of immune cells, and salt-sensitive hypertension: all for one and one for all Am J Physiol Renal Physiol, April 1, 2004; 286(4): F606 - F616. [Abstract] [Full Text] [PDF]
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A. Nishiyama, L. Yao, Y. Nagai, K. Miyata, M. Yoshizumi, S. Kagami, S. Kondo, H. Kiyomoto, T. Shokoji, S. Kimura, et al. Possible Contributions of Reactive Oxygen Species and Mitogen-Activated Protein Kinase to Renal Injury in Aldosterone/Salt-Induced Hypertensive Rats Hypertension, April 1, 2004; 43(4): 841 - 848. [Abstract] [Full Text] [PDF]
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M. Asghar and M. F. Lokhandwala Antioxidant Supplementation Normalizes Elevated Protein Kinase C Activity in the Proximal Tubules of Old Rats Experimental Biology and Medicine, March 1, 2004; 229(3): 270 - 275. [Abstract] [Full Text] [PDF]
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A. Nishiyama, M. Yoshizumi, H. Hitomi, S. Kagami, S. Kondo, A. Miyatake, M. Fukunaga, T. Tamaki, H. Kiyomoto, M. Kohno, et al. The SOD Mimetic Tempol Ameliorates Glomerular Injury and Reduces Mitogen-Activated Protein Kinase Activity in Dahl Salt-Sensitive Rats J. Am. Soc. Nephrol., February 1, 2004; 15(2): 306 - 315. [Abstract] [Full Text] [PDF]
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S. H. Mehta, R. C. Webb, A. Ergul, A. Tawak, and A. M. Dorrance Neuroprotection by tempol in a model of iron-induced oxidative stress in acute ischemic stroke Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2004; 286(2): R283 - R288. [Abstract] [Full Text] [PDF]
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J. Zhu, T. Mori, T. Huang, and J. H. Lombard Effect of high-salt diet on NO release and superoxide production in rat aorta Am J Physiol Heart Circ Physiol, February 1, 2004; 286(2): H575 - H583. [Abstract] [Full Text] [PDF]
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H. Xu, G. D. Fink, and J. J. Galligan Tempol Lowers Blood Pressure and Sympathetic Nerve Activity But Not Vascular O2- in DOCA-Salt Rats Hypertension, February 1, 2004; 43(2): 329 - 334. [Abstract] [Full Text] [PDF]
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S. Adler, H. Huang, M. S. Wolin, and P. M. Kaminski Oxidant Stress Leads to Impaired Regulation of Renal Cortical Oxygen Consumption by Nitric Oxide in the Aging Kidney J. Am. Soc. Nephrol., January 1, 2004; 15(1): 52 - 60. [Abstract] [Full Text] [PDF]
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P. Minuz, P. Patrignani, S. Gaino, F. Seta, M. L. Capone, S. Tacconelli, M. Degan, G. Faccini, A. Fornasiero, G. Talamini, et al. Determinants of Platelet Activation in Human Essential Hypertension Hypertension, January 1, 2004; 43(1): 64 - 70. [Abstract] [Full Text] [PDF]
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C. Kitiyakara, T. Chabrashvili, Y. Chen, J. Blau, A. Karber, S. Aslam, W. J. Welch, and C. S. Wilcox Salt Intake, Oxidative Stress, and Renal Expression of NADPH Oxidase and Superoxide Dismutase J. Am. Soc. Nephrol., November 1, 2003; 14(11): 2775 - 2782. [Abstract] [Full Text] [PDF]
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M. H. Sedeek, M. T. Llinas, H. Drummond, L. Fortepiani, S. R. Abram, B. T. Alexander, J. F. Reckelhoff, and J. P. Granger Role of Reactive Oxygen Species in Endothelin-Induced Hypertension Hypertension, October 1, 2003; 42(4): 806 - 810. [Abstract] [Full Text] [PDF]
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J. A. Payne, J. F. Reckelhoff, and R. A. Khalil Role of oxidative stress in age-related reduction of NO-cGMP-mediated vascular relaxation in SHR Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2003; 285(3): R542 - R551. [Abstract] [Full Text] [PDF]
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M. Tepel Oxidative stress: does it play a role in the genesis of essential hypertension and hypertension of uraemia? Nephrol. Dial. Transplant., August 1, 2003; 18(88): 1439 - 1442. [Full Text]
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T. Chabrashvili, C. Kitiyakara, J. Blau, A. Karber, S. Aslam, W. J. Welch, and C. S. Wilcox Effects of ANG II type 1 and 2 receptors on oxidative stress, renal NADPH oxidase, and SOD expression Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2003; 285(1): R117 - R124. [Abstract] [Full Text] [PDF]
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S. Racasan, J. A. Joles, P. Boer, H. A. Koomans, and B. Braam NO dependency of RBF and autoregulation in the spontaneously hypertensive rat Am J Physiol Renal Physiol, July 1, 2003; 285(1): F105 - F112. [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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C. Zhang, T. W. Hein, W. Wang, and L. Kuo Divergent Roles of Angiotensin II AT1 and AT2 Receptors in Modulating Coronary Microvascular Function Circ. Res., February 21, 2003; 92(3): 322 - 329. [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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T. Ogihara, T. Asano, K. Ando, Y. Chiba, H. Sakoda, M. Anai, N. Shojima, H. Ono, Y. Onishi, M. Fujishiro, et al. Angiotensin II-Induced Insulin Resistance Is Associated With Enhanced Insulin Signaling Hypertension, December 1, 2002; 40(6): 872 - 879. [Abstract] [Full Text] [PDF]
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 Y. Sun, J. Zhang, L. Lu, S. S. Chen, M. T. Quinn, and K. T. Weber Aldosterone-Induced Inflammation in the Rat Heart : Role of Oxidative Stress Am. J. Pathol., November 1, 2002; 161(5): 1773 - 1781. [Abstract] [Full Text] [PDF]
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S. Meng, L. J. Roberts II, G. W. Cason, T. S. Curry, and R. D. Manning Jr. Superoxide dismutase and oxidative stress in Dahl salt-sensitive and -resistant rats Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2002; 283(3): R732 - R738. [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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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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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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T. Aizawa, N. Ishizaka, S.-I. Usui, N. Ohashi, M. Ohno, and R. Nagai Angiotensin II and Catecholamines Increase Plasma Levels of 8-Epi-Prostaglandin F2{alpha} With Different Pressor Dependencies in Rats Hypertension, January 1, 2002; 39(1): 149 - 154. [Abstract] [Full Text] [PDF]
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