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(Circulation. 1998;97:2197-2201.)
© 1998 American Heart Association, Inc.

Brief Rapid Communication

Estrogen Modulates AT₁ Receptor Gene Expression In Vitro and In Vivo

Georg Nickenig, MD; Anselm T. Bäumer, MD; Christian Grohè, MD; Stefan Kahlert, PhD; Kerstin Strehlow, MS; Stephan Rosenkranz, MD; Alexander Stäblein, MD; Frank Beckers, MS; Jos F. M. Smits, MD; Mat J. A. P. Daemen, MD; Hans Vetter, MD; ; Michael Böhm, MD

From the Klinik III für Innere Medizin, Universität zu Köln (G.N., A.T.B., K.S., S.R., A.S., F.B., M.B.), and the Medizinische Universitäts-Poliklinik, Bonn (C.G., S.K., H.V.), Germany; and the Departments of Pharmacology (J.F.M.S.) and Pathology (M.J.A.P.D.), Cardiovascular Research Institute, University of Maastricht, the Netherlands. Drs Nickenig and Bäumer contributed equally to this study.

Correspondence to Dr Georg Nickenig, Klinik III für Innere Medizin, Joseph-Stelzmann-Str 9, 50924 Köln, Germany. E-mail georg.nickenig{at}uni-koeln.de

Abstract

Background—The AT₁ receptor has been implicated in the pathogenesis of hypertension and atherosclerosis. Estrogen deficiency is also associated with cardiovascular diseases. Therefore, we examined the AT₁ receptor gene expression in ovariectomized rats with and without estrogen replacement therapy and the influence of estrogen on AT₁ receptor expression in cultured vascular smooth muscle cells.

Methods and Results—Rat aortic tissue was examined 5 weeks after ovariectomy. In one group, estrogen (1.7 mg estradiol) was administered during the 5-week period. Functional experiments assessed angiotensin II–induced contraction of aortic rings. AT₁ receptor mRNA levels were measured by quantitative polymerase chain reaction and Northern blotting. AT₁ receptor density was assessed by radioligand binding assays. These techniques were also applied in cultured vascular smooth muscle cells. The efficacy of angiotensin II on vasoconstriction was significantly increased in aortas from ovariectomized rats. As assessed by radioligand binding assays, AT₁ receptor density was increased to 160% without changes in receptor affinity during estrogen deficiency. AT₁ receptor mRNA levels were consistently increased to 187% in ovariectomized rats compared with sham-operated animals. Estrogen substitution therapy in ovariectomized rats reversed this AT₁ receptor overexpression. To explore the underlying mechanisms, the direct influence of estradiol on AT₁ receptor expression was investigated in VSMCs. Estradiol (1 µmol/L) led to a time-dependent downregulation of AT₁ receptor mRNA, with a maximum of 33.3% at 12 hours. There was a correlative decrease in AT₁ receptor density.

Conclusions—This novel observation of estrogen-induced downregulation of AT₁ receptor expression could explain the association of estrogen deficiency with hypertension and atherosclerosis, because activation of the AT₁ receptor plays a key role in the regulation of blood pressure, fluid homeostasis, and vascular cell growth.

Key Words: angiotensin • hypertension • hormones • genes • muscle, smooth • atherosclerosis

The low incidence of vascular diseases in premenopausal women and the rapid increase of the risk of cardiovascular events after menopause as well as the beneficial effects of estrogen replacement therapy on cardiac and vascular morbidity have suggested a important role of estrogens in the pathogenesis of atherosclerosis.^{1 2 3} In addition to its effects on classic cardiovascular risk factors, eg, in the sense of a decrease of cholesterol plasma levels,^{4 5} estrogen has been recognized to directly influence vascular as well as myocardial cells. Indeed, VSMCs, myocytes, and cardiac fibroblasts have been shown to contain functional estrogen receptors.^{6 7 8} Moreover, there is increasing evidence that estrogen interferes with the RAS. The production of angiotensinogen is enhanced, whereas ACE levels are decreased, by estrogens.⁹ According to a recent report, plasma renin levels are also reduced during estrogen replacement therapy, but other reports suggested either an increase or no change of plasma renin levels on estrogen treatment.^{10 11 12 13} One of the major components of the RAS is the AT₁ receptor, which mediates most biological effects of Ang II, such as vasoconstriction, aldosterone release, sodium and water retention, and cellular growth.¹⁴ The expression level of the AT₁ receptor is subject to regulation and governs the activity of the entire RAS through upregulation or downregulation. The AT₁ receptor is regulated by, eg, lipoproteins, growth factors, and Ang II in vitro as well as in vivo, suggesting the important role of this receptor in the development of atherosclerosis.^{15 16 17 18} To explore a potential involvement of AT₁ receptor regulation in the estrogen-induced modulation of cardiovascular diseases, we investigated the effects of estrogen deficiency on vascular AT₁ receptor expression in ovariectomized rats and the direct effect of estradiol on AT₁ receptor expression in VSMCs.

Methods

Animals
Wistar-Kyoto rats were ovariectomized or sham-operated 8 weeks after birth. Tissue samples were harvested 5 weeks after surgery. For treatment, 17-estradiol pellets (containing 1.7 mg estradiol each, 60-day release, Innovative Research) were subcutaneously administered with a 10-gauge trochar. Plasma estrogen and renin levels were measured by standardized procedures (Amersham kit).

Functional Experiments
Rats were killed by decapitation 4 weeks after operation. Then the chest was rapidly opened, and the descending thoracic aorta was removed. The aorta was placed in chilled Krebs-Henseleit buffer and cleaned of excessive adventitial tissue. Eight 2- to 5-mm ring segments of thoracic aorta were suspended in individual organ chambers.¹⁸ When a stable baseline tone was established, potassium chloride, norepinephrine, endothelin, and Ang II were added at the concentrations indicated, interrupted by washout periods.

Cell Culture
VSMCs were isolated from rat thoracic aorta (female Wistar-Kyoto, 6 to 10 weeks old) by enzymatic dispersion as described previously.¹⁷ Cells were grown in a 5% CO₂ atmosphere at 37°C in estrogen-free and phenol-free DMEM supplemented with 100 U/mL penicillin, 100 µg/mL streptomycin, 1% nonessential amino acids (x100), and 10% estrogen-free FCS.

mRNA Isolation, Northern Analysis, Quantitative PCR
After the indicated treatments, cells or isolated aortas were lysed with RNA-clean (AGS) and processed according to the manufacturer's protocol to obtain total cellular RNA. Aliquots (10 µg) were electrophoresed through formaldehyde agarose gels, transferred onto Hybond N membranes, and then hybridized for 15 hours at 42°C with a random-primed, [³²P]dCTP-labeled rat AT₁ receptor cDNA probe as described previously in detail.¹⁷ For quantitative PCR, isolated RNA was analyzed with a deletion-mutated AT₁ receptor mRNA as internal standard. PCR was performed under the same conditions and with use of the same specific primers as described previously.¹⁹

Radioligand Binding Assays
VSMCs and aortic tissue were homogenized and membranes were isolated as described elsewhere.¹⁸ Ang II receptors were investigated in saturation experiments using ¹²⁵I-labeled Ang II as radiolabeled ligand. The AT₁ receptor antagonist DUP 753 (10 µmol/L) was used to determine nonspecific binding. The incubation was carried out at 24°C for 60 minutes. All experiments were performed in triplicate. The maximal density (B_max) and apparent affinity (K_d) of binding sites were obtained from nonlinear regression analysis.

Statistical Analysis
Data are presented as mean±SEM. Statistical analysis was performed by the one-factor ANOVA test using the Scheffé procedure.

Results

Plasma estradiol concentrations were significantly lower in male (7.7±0.8 pg/mL; P<0.05) and female ovariectomized (3.0±0.3 pg/mL; P<0.05) rats than in sham-operated female animals (49.6±11.9 pg/mL). Blood pressure levels were not significantly different between the tested groups (data not shown).

To examine the functional response of aortas isolated from sham-operated female rats, ovariectomized rats, and male rats, aortic constriction experiments were performed in the presence of various agonists. Vasoconstriction induced by 60 mmol/L potassium chloride was not significantly different between groups (data not shown). Ang II caused a significantly stronger vasoconstriction in ovariectomized rats versus sham-operated rats, which was comparable to that of male rats (Figure 1A). The maximal constriction was increased in female rats from 12.8±1.6% to 17.4±1.1% (P<0.05) of KCl-induced vasoconstriction in ovariectomized female rats (18.3±1.6% in male rats). The EC₅₀ values were not significantly altered. Control experiments using 0.1 nmol/L to 10 µmol/L phenylephrine and 10 nmol/L endothelin showed no significant difference between groups for either agonist (Figure 1B and 1C). The following experiments were conducted to clarify whether this profound increase in Ang II–caused vasoconstriction was based on increased AT₁ receptor expression. Quantitative PCR techniques showed that AT₁ receptor mRNA steady-state levels were significantly enhanced in aortas isolated from ovariectomized rats versus sham-operated rats. AT₁ receptor mRNA levels were comparable in male rats and ovariectomized female rats (Figure 1D). GAPDH mRNA was measured similarly in all groups (data not shown). Consequently, AT₁ receptor density was significantly increased in ovariectomized rats compared with sham-operated rats. B_max values were enhanced to 6.3±0.4 fmol/mg protein during estrogen deficiency versus 4.0±0.5 fmol/mg protein in normal female animals. The receptor affinities were not significantly different (K_d, 1.1 nmol/L [0.6 to 1.6 nmol/L] in ovariectomized versus 1.1 nmol/L [0.2 to 1.9 nmol/L] in sham-operated rats).

View larger version (41K): [in this window] [in a new window]   Figure 1. Functional effects of Ang II and AT1 receptor expression in ovariectomized rats. Force of contraction in response to increasing concentrations of Ang II (A), phenylephrine (B), and 10 nmol/L endothelin (C) in aortic rings isolated from female ovariectomized, female sham-operated, and male rats. Each point represents mean±SEM, n=10, *P<0.05. D, AT1 receptor mRNA levels in aortas from female ovariectomized, female sham-operated, and male rats as assessed by quantitative PCR. AT1 receptor mRNA steady-state levels are expressed as ratio between wild-type and internal standard AT1 receptor. Each point represents mean±SEM, n=5, *P<0.05. E, AT1 receptor mRNA levels in aortas from female ovariectomized, female sham-operated, and female ovariectomized rats with estrogen treatment as assessed by quantitative PCR. AT1 receptor mRNA steady-state levels are expressed as ratio between wild-type and internal standard AT1 receptor mRNA.

Renin plasma levels were measured to assess a possible compensatory modulation of the circulating RAS in response to the marked AT₁ receptor overexpression. Indeed, renin concentrations were significantly lower in ovariectomized female rats (18.5±0.7 ng/mL) than in sham-operated female rats (23.3±1.8 ng/mL; P<0.05). Control experiments were conducted in which ovariectomized rats were substituted with exogenous estrogen. Figure 1E illustrates that aortic AT₁ receptor mRNA was downregulated to control levels in ovariectomized female animals after estrogen treatment, suggesting a decisive role for estrogens in gene regulation of the vascular AT₁ receptor. GAPDH mRNA remained unchanged (data not shown).

Most if not all vascular AT₁ receptors are expressed in VSMCs, and AT₁ receptor–mediated growth and vasoconstriction are realized predominantly through this cell type.¹⁴ To gain further mechanistic insight into the in vivo AT₁ receptor regulation during estrogen deficiency, we investigated the effects of estradiol on VSMCs in culture. Control experiments showed that AT₁ receptor and GAPDH mRNA levels remain stable over the experimental period of 24 hours (Figure 2A). Estradiol (1 µmol/L) caused downregulation of AT₁ receptor mRNA levels, with a maximal effect of 33.3±11% after a 12-hour incubation (Figure 2B). Radioligand binding assays on cells treated for 12 hours with estradiol confirmed that, like the AT₁ receptor mRNA, the AT₁ receptor density was significantly downregulated from B_max values of 1327.3±183.3 fmol/mg protein in controls to 776.9±49.5 fmol/mg protein in estradiol-treated cells (Figure 2C). The receptor affinity was not significantly different (K_d=1.7 nmol/L [1.1 to 2.2 nmol/L] versus 2.7 nmol/L [1.2 to 4.2 nmol/L]).

View larger version (20K): [in this window] [in a new window]   Figure 2. Effect of estradiol on AT1 receptor expression in VSMCs. A and B, AT1 receptor steady-state levels. Time course of AT1 receptor () and GAPDH mRNA () in the presence of either vehicle (A) or 1 µmol/L estradiol (B) in VSMCs. Northern hybridizations were performed as described in "Methods." Each point represents relative hybridization signal (mean±SEM) normalized to 0-hour treatment with vehicle (100%) from 5 separate experiments. C, AT1 receptor density. Confluent cells were exposed to either 1 µmol/L estradiol () or vehicle (). Saturation binding assays using [125I]-labeled Ang II were performed on isolated membranes. AT1 receptor antagonist Dup753 (10 µmol/L) was used to define nonspecific binding. Each curve represents specific binding of radioligand (cpm radioligand bound minus cpm bound in the presence of 10 µmol/L losartan). Kd and Bmax values reported in the text were derived from nonlinear regression of specific bound versus free data. Each point represents binding data of 3 independent experiments ±SEM.

Discussion

Estrogen deficiency leads to upregulation of vascular AT₁ receptor expression accompanied by an increased effect of Ang II on tension in isolated aortic rings. This is presumably based on a direct downregulating effect of estradiol on AT₁ receptor gene expression in VSMCs.

VSMCs play a central role in the pathogenesis of atherosclerosis.²⁰ Both estrogen and AT₁ receptors are expressed in this cell type; therefore, estrogens and Ang II may influence the intracellular processes of VSMCs.^{6 14} The AT₁ receptor decisively controls the events involved in VSMC growth and vasoconstriction.²¹ Because this receptor is subjected to homologous and heterologous regulation, its expression level governs the efficacy of the entire RAS. It is therefore conceivable that modulation of AT₁ receptor expression may lead to acceleration of pathophysiological events involved in the development of vascular disease.

In addition, estrogens putatively participate in the atherosclerotic process suggested by the rapid increase of vascular events in women after menopause.^{1 2 3} Several mechanisms have been proposed that may initiate this atheroprotective effect of estrogens. Among others, beneficial influence on classic risk factors,^{4 5} scavenging of free radicals,²² and interference with the RAS have been reported. In this context, enhanced production of angiotensinogen^{10 11} and reduced levels of ACE^{13 23} have been observed, whereas the effect of estrogens on renin are the subject of ongoing controversy.^{10 13 23}

In ovariectomized rats, estrogen deficiency causes vascular overexpression of the AT₁ receptor. In this short-term model, the blood pressure is not elevated significantly, probably because of the compensatory decrease of circulating renin levels. Our findings suggest that estrogen directly modulates AT₁ receptor expression in VSMCs.

Recent reports showed that the AT₁ receptor is overexpressed during conditions that are known to be associated with increased incidence of hypertension and atherosclerosis. LDL and salt cause a significant upregulation of AT₁ receptor gene expression, leading to an enhanced biological efficacy of Ang II.^{17 18 24} Hypercholesterolemia and increased salt load not only lead to an accelerated progression of cardiovascular diseases but also are associated with overexpression of AT₁ receptors, indicating that this receptor regulation may indeed participate decisively in the development of hypertension and atherosclerosis. In analogy, the incidence of hypertension and atherosclerosis is increased in estrogen-deficient women,^{1 2 3} possibly because of increased vasoconstriction and cell growth via overexpressed AT₁ receptors. Estrogen replacement therapy causes a decreased risk for cardiovascular diseases; AT₁ receptors are consistently downregulated by estrogens. Therefore, it may be concluded that upregulation of AT₁ receptors during estrogen deficiency and the premenopausal, physiological "downregulation" of AT₁ receptors are involved in the estrogen-driven effects on onset and development of hypertension and atherosclerosis.

Selected Abbreviations and Acronyms

Ang II = angiotensin II PCR = polymerase chain reaction RAS = renin-angiotensin system VSMC = vascular smooth muscle cell

Acknowledgments

This work was supported by the Deutsche Forschungsgemeinschaft. The technical assistance of Marc Wolff and Kerstin Löbbert is greatly appreciated.

Received March 4, 1998; revision received April 7, 1998; accepted April 16, 1998.

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