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Regulation of Angiotensin II Type 2 Receptor Gene Expression in the Adrenal Medulla by Acute and Repeated Immobilization Stress

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Regulation of Angiotensin II Type 2 Receptor Gene Expression in the Adrenal Medulla by Acute and Repeated Immobilization Stress 291 Regulation of angiotensin II type 2 receptor gene expression in the adrenal medulla by acute and repeated immobilization stress Regina Nostramo, Andrej Tillinger, Juan M Saavedra1, Ashok Kumar2,†, Varunkumar Pandey2,†, Lidia Serova, Richard Kvetnansky3 and Esther L Sabban Department of Biochemistry and Molecular Biology, New York Medical College, Valhalla, New York 10595, USA 1Section of Pharmacology, DIRP, National Institute of Mental Health, NIH, Bethesda, Maryland 20892, USA 2Department of Pathology, New York Medical College, Valhalla, New York 10595, USA 3Institute of Experimental Endocrinology, Slovak Academy of Sciences, Bratislava, Slovakia (Correspondence should be addressed to E L Sabban; Email: [email protected]) †(A Kumar and V Pandey are now at Department of Physiology and Pharmacology, University of Toledo College of Medicine, Toledo, Ohio, USA) Abstract While the renin–angiotensin system is important for of stress-triggered activation of the hypothalamic–pituitary– adrenomedullary responses to stress, the involvement of adrenocortical or sympathoadrenal axis in AT2 receptor specific angiotensin II (Ang II) receptor subtypes is unclear. downregulation was examined. Cultured cells treated with We examined gene expression changes of angiotensin II the synthetic glucocorticoid dexamethasone displayed a type 1A (AT1A) and type 2 (AT2) receptors in rat adrenal transcriptionally mediated decrease in AT2 receptor mRNA medulla in response to immobilization stress (IMO). AT2 levels. However, glucocorticoids are not required for the receptor mRNA levels decreased immediately after a single immediate stress-triggered decrease in AT2 receptor gene 2-h IMO. Repeated IMO also decreased AT2 receptor expression, as demonstrated in corticotropin-releasing mRNA levels, but the decline was more transient. AT1A hormone knockout (Crh KO) mice and hypophysectomized receptor mRNA levels were unaltered with either single or rats, although they can regulate basal gene expression. repeated IMO, although binding was increased following cAMP and pituitary adenylate cyclase-activating polypeptide repeated IMO. These effects of stress on Ang II receptor also reduced AT2 receptor gene expression and may mediate expression may alter catecholamine biosynthesis, as tyrosine this response. Overall, the effects of stress on adreno- hydroxylase and dopamine b-hydroxylase mRNA levels in medullary AT1A and AT2 receptor expression may con- PC12 cells are decreased with Ang II treatment in the tribute to allostatic changes, such as regulation of presence of ZD7155 (AT1 receptor antagonist) or with catecholamine biosynthesis. CGP42112 (AT2 receptor agonist) treatment. Involvement Journal of Endocrinology (2012) 215, 291–301 Introduction et al. (2009)). The renin–angiotensin system (RAS), which is known for regulating blood pressure and fluid and The response of an organism to acute stress is necessary for electrolyte balance, also plays an important role in the stress survival. However, when stress is prolonged or repeated, the response (reviewed in Saavedra et al. (2011) and Saavedra response is not only adaptive but also becomes maladaptive. (2012)). Levels of plasma renin as well as circulating and With repeated exposure to stress, there is an increase in adrenal angiotensin II (Ang II), the main active component allostatic load (McEwen & Seeman 1999, McEwen 2007). of the RAS, are elevated in response to stress ( Jindra As a result, stress is a major contributor to the development & Kvetnansky´ 1982, Yang et al. 1993). The RAS likely of cardiovascular disorders and neuropsychiatric illnesses and contributes to the development of stress-related cardio- can also adversely influence the progression of chronic vascular disorders (Saavedra et al.2011); however, the diseases, such as diabetes and cancer (reviewed in McEwen underlying mechanisms are still unclear. (1998) and Chrousos (2009)). Ang II is a potent secretagogue that stimulates adreno- The physiological responses to stress involve multiple medullary norepinephrine and epinephrine release (Feldberg systems. The activation of the hypothalamic–pituitary– & Lewis 1964). Accordingly, nephrectomy or treatment with adrenocortical (HPA) axis and the catecholaminergic a nonselective Ang II receptor antagonist nearly abrogates sympathoneural and sympathoadrenal systems is key catecholamine release from cat adrenal medulla in neuroendocrine responses to stress (reviewed in Kvetnansky response to the stress of insulin-induced hypoglycemia Journal of Endocrinology (2012) 215, 291–301 DOI: 10.1530/JOE-12-0181 0022–0795/12/0215–291 q 2012 Society for Endocrinology Printed in Great Britain Online version via http://www.endocrinology-journals.org Downloaded from Bioscientifica.com at 09/24/2021 11:31:41AM via free access 292 R NOSTRAMO and others . Stress and adrenomedullary AT2 receptor (Bumpus et al. 1980). Ang II also induces catecholamine Liu et al. 2008). The findings reveal a biphasic response of biosynthesis by elevating gene expression of the catechol- AT2 receptor gene expression to stress and provide insight amine biosynthetic enzymes, tyrosine hydroxylase (TH), into the mechanisms that trigger these dramatic changes. and phenylethanolamine N-methyltransferase (PNMT) (Stachowiak et al. 1990b). The results may depend on which Ang II receptor subtype is involved. Ang II binds with equal affinity to two major sites, the Materials and methods angiotensin II type 1 (AT ) and type 2 (AT ) receptors 1 2 Animals (reviewed in de Gasparo et al. (2000)). In rodents, there are two subtypes of AT1 receptor, the AT1A and AT1B receptor, All animal experiments were performed in accordance with which are pharmacologically indistinguishable but differen- the NIH Guide for the Care and Use of Laboratory Animals tially regulated (reviewed in Inagami et al. (1994)). The (NIH publication no. 85-23, revised 1996) and were AT1 receptors mediate virtually all the well-known effects of approved by the NYMC Institutional Animal Care and Use Ang II, including vasoconstrictive, hypertrophic, prolifera- Committee (rat experiments) or the Ethical Committee of tive, and pro-fibrotic effects. Although the expression of the Institute of Experimental Endocrinology, Slovak Acad- AT1 receptors in rodent adrenal medulla is very low and emy of Sciences (mouse experiments). limited to only the AT1A receptor subtype (Leong et al. 2002), Male, Sprague Dawley rats (250–320 g) were obtained there is substantial evidence for a role of AT1 receptors in from Taconic Farms (Germantown, NY, USA). Male, maintaining basal adrenomedullary catecholamine synthesis corticotropin-releasing hormone knockout (Crh KO) and in mediating central and adrenomedullary responses mice (C57B1/129SV) and WT mice, age 150–180 days, to stress (Armando et al. 2001, 2007, Leong et al. 2002, were bred at the Institute of Experimental Endocrinology, as Jezova et al. 2003). described previously (Kvetnansky et al. 2006). The Crh KO AT2 receptor activation has been proposed to oppose AT1 mouse line was originally a generous gift from Dr Joseph A receptor-mediated effects and is associated with vasodilation; Majzoub (Harvard Medical School, Department of Endo- nitric oxide release; and anti-hypertrophic, anti-proliferative, crinology, Boston, MA, USA). The animals were maintained and anti-fibrotic effects (reviewed in de Gasparo et al. under controlled conditions (23G2 8C, 12 h light:12 h (2000)). Multiple in vivo studies using genetically altered darkness cycle, lights on from 0600 h) with food and water animals or selective pharmacological agents suggest tissue ad libitum. protective properties of the AT2 receptor subtype in a number Hypophysectomized or sham-operated rats (Taconic of disease states (reviewed in Jones et al. (2008)). Unlike Farms) were administered saline or 25 mg/kg per day the AT1 receptor, the AT2 receptor is not very abundant (1 ml/h) hydrocortisone 21-hemisuccinate, sodium salt in adult tissues, except for the adrenal gland where it is crystalline (cortisol; Sigma–Aldrich Corp.) for 7 days via highly expressed in the zona glomerulosa and medulla osmotic minipump inserted s.c. in the interscapular area. (Israel et al. 1995). All hypophysectomized rats received isotonic saline instead While Ang II elevates TH gene expression in primary of drinking water. Complete removal of the pituitary in cultures of bovine adrenomedullary cells (Stachowiak et al. hypophysectomized rats was visually confirmed. 1990b), more recently it was shown that activation of the AT2 receptor inhibits catecholamine synthesis and TH expression Stress and activity in porcine adrenomedullary chromaffin cells (Takekoshi et al. 2000, 2002). AT2 receptor gene-deficient IMO, a strong noninvasive stress model, was performed as mice show elevated adrenomedullary Th and AT1 receptor described previously (Nankova et al. 1994, Liu et al. 2008)on mRNA levels, norepinephrine and epinephrine levels, as well a metal board by taping the limbs with surgical tape and as enhanced HPA axis stimulation (Saavedra et al. 2001, restricting the motion of the head exactly as originally Armando et al. 2002). This indicates that the AT1 and AT2 described by Kvetnansky & Mikulaj (1970). Rats were receptors may play opposite roles in the regulation of the subjected to single or repeated IMO. For single IMO (1! adrenomedullary response to stress and that the expression of IMO), rats were immobilized once for 2 h and subsequently one receptor type may influence the expression of the other. killed either immediately
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