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Antidepressant Effects of Abscisic Acid Mediated by the Downregulation Of International Journal of Neuropsychopharmacology, 2014, 1–9 doi:10.1093/ijnp/pyu006 Research Article research article Antidepressant Effects of Abscisic Acid Mediated by the Downregulation of Corticotrophin-Releasing Hormone Gene Expression in Rats Cong-Cong Qi, MD; Zhi Zhang, MD; Hui Fang, MD; Ji Liu, MD; Nan Zhou, MD; Jin-Fang Ge, MD; Fang-Han Chen, MD; Cheng-Bin Xiang, MD; Jiang-Ning Zhou, MD, PhD CAS Key Laboratory of Brain Function and Diseases, Schol of Life Science, University of Science and Technology of China, Anhui, China (Drs Qi, Zhang, Fang, Liu, Ge, Chen, and J-N Zhou); Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai, China (Dr N Zhou); Plant Molecular Biology Laboratory, School of Life Science, University of Science and Technology of China, Anhui, China (Dr Xiang). Correspondence: Jiang-Ning Zhou, MD, PhD, School of Life Science, University of Science and Technology of China, Huangshan Road 443, Hefei 230027, Anhui, China ([email protected]). Background: Corticotrophin-releasing hormone (CRH) is considered to be the central driving force of the hypothalamic- pituitary-adrenal axis, which plays a key role in the stress response and depression. Clinical reports have suggested that excess retinoic acid (RA) is associated with depression. Abscisic acid (ABA) and RA are direct derivatives of carotenoids and share a similar molecular structure. Here, we proposed that ABA also plays a role in the regulation of CRH activity sharing with the RA signaling pathway. Methods: [3H]-ABA radioimmunoassay demonstrated that the hypothalamus of rats shows the highest concentration of ABA compared with the cortex and the hippocampus under basal conditions. Results: Under acute stress, ABA concentrations increased in the serum, but decreased in the hypothalamus and were accompanied by increased corticosterone in the serum and c-fos expression in the hypothalamus. Moreover, chronic ABA administration increased sucrose intake and decreased the mRNA expression of CRH and retinoic acid receptor alpha (RARα) in the hypothalamus of rats. Furthermore, ABA improved the symptom of chronic unpredictable mild stress in model rats, as indicated by increased sucrose intake, increased swimming in the forced swim test, and reduced mRNA expression of CRH and RARα in the rat hypothalamus. In vitro, CRH expression decreased after ABA treatment across different neural cells. In BE(2)-C cells, ABA inhibited a series of retinoid receptor expression, including RARα, a receptor that could facilitate CRH expression directly. Conclusions: These results suggest that ABA may play a role in the pathogenesis of depression by downregulating CRH mRNA expression shared with the RA signaling pathway. Keywords: abscisic acid, corticotrophin-releasing hormone, depression, retinoic acid receptor alpha, stress response Introduction The hypothalamic-pituitary-adrenal (HPA) axis is considered to Corticotrophin-releasing hormone (CRH) in the paraventricular be the final common pathway in the stress response and the nucleus of the hypothalamus plays a central role in the regula- symptoms of depression (Swaab et al., 2005; Bao et al., 2008). tion of HPA axis activity (Swaab, 1995; Bao et al., 2006). Evidence Received: May 15, 2014; Revised: August 07, 2014; Accepted: August 25, 2014 © The Author 2014. Published by Oxford University Press on behalf of CINP. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, 1 provided the original work is properly cited. For commercial re-use, please contact [email protected] 2 | International Journal of Neuropsychopharmacology, 2014 from abundant clinical case reports uncovered the association For the animals that received an intraperitoneal injec- between retinoic acid (RA) treatment and depressive symptoms tion, (±)-cis, trans-ABA (Sigma), and fluoxetine hydrochloride (Bremner and McCaffery, 2008; Bremner et al., 2012). Recently, (Sigma) were dissolved in a vehicle of sterile saline solution we have demonstrated that retinoic acid receptor alpha (RARα) (0.9% w/v sodium chloride) with dimethyl sulfoxide at a ratio contributes to the etiology of affective disorder through co- of 1:1 (v/v). localized and upregulated CRH gene expression (Chen et al., 2009). Moreover, chronic RA administration induces HPA axis Acute Stress hyperactivity and depression-like behavioral changes in young rats (Cai et al., 2010). Direct intracerebroventricular injection of Two-month-old SD rats (250–300 g) were randomly divided into RA induces potent HPA axis activation and typical depression- two groups: the handled control (n=20) and the forced swim test like behaviors in rats (Hu et al., 2013). Furthermore, abnormal (FST; n=20) groups. The 15-min FST for the rats was conducted endogenous retinoid signaling has also been found in the brains by placing each rat in a cylinder (60 cm x 30 cm) containing water of depressed patients (Chen et al., 2009; Qi et al., 2013). These at 22 ± 2◦C with a depth of 35 cm. The control rats were simulta- findings suggest that the RA signaling pathway may be involved neously handled for 5 min and kept away from the FST to avoid in the pathophysiology of depression. Interestingly, abscisic acid stress. The rats were anesthetized and decapitated immediately (ABA) and RA are direct derivatives of carotenoids (Vershinin, after the FST. 1999; Nambara and Marion-Poll, 2005), and both substances share a similar molecular structure: the free carboxyl group at Chronic ABA Administration in SD Young Rats and the end of the isoprene-composed side chain, which is a criti- the Behavior Test cal part of their bioactivity (Bremner and McCaffery, 2008; Moise et al., 2009). Whether ABA also plays a role in regulating the activ- The four-week-old SD rats received a daily injection of 20 mg/ ity of CRH sharing with RA signaling pathway remains unclear. kg ABA (n=7) or the vehicle (control, n=6) treatment; the ani- ABA is a crucial phytohormone that exists and functions mals were continuously treated between 0800 and 1000 h for not only in plants, fungi, cyanobacteria, and algae, but also in six weeks before the behavioral test. All rats were housed indi- a wide range of lower animals and mammals, including vari- vidually for 24 h prior to the sucrose intake test. The rats were ous human tissues and cells (Cowan and Rose, 1991; Bruzzone deprived of water and food for 12 h and then given one bottle et al., 2007; Nagamune et al., 2008; Li et al., 2011; Bruzzone of 1% sucrose and one bottle of water at the same time; the et al., 2012). Recently, ABA was identified as an endogenous positions of the bottles were random. The amount of each solu- hormone in mammals, which acts as a stress signal and tion consumed was determined by weighing the bottles before regulates different cell functions, including inflammatory and after the 12 h consumption period. The sucrose intake was processes, stem cell expansion, insulin release, and glucose calculated as the sucrose consumed (g)/the body weight (kg) of uptake (Bruzzone et al., 2008; Scarfi et al., 2008; Bodrato et al., each rat (Duncko et al., 2001). 2009; Bruzzone et al., 2012). Moreover, dietary ABA ameliorates glucose tolerance and obesity-related inflammation in db/db ABA Administration in the CUMS Model Rats and mice (Guri et al., 2007; Guri et al., 2010a), decreases intestinal the Behavior Test inflammation in mouse models of inflammatory bowel disease (Guri et al., 2010b; Guri et al., 2011), and reduces pulmonary The chronic unpredictable mild stress model was used as a vali- inflammation in mouse models of influenza virus–associated dated animal model of depression. The three weeks CUMS proto- disease (Hontecillas et al., 2012). Interestingly, Le Page-Degivry col and the behavior tests to measure the depression behaviors et al. (1986) first reported the presence of ABA in the mamma- were performed as described previously (Wu et al., 2007; Ge et al., lian brain and other tissues; clearly, the brain contained much 2013). Forty-five SD rats (seven weeks old) were randomly split more ABA than any other types of tissue. Despite these find- into four groups, including an undisrupted control group (vehicle ings, further insight into ABA functions in the brain and the control, n=12), a chronic unpredictable mild stress group (vehi- central nervous system (CNS) is lacking. The distribution of cle + CUMS, n=11), a fluoxetine-treated group (2 mg/kg/day Flu ABA in the brains of rodents and its role in the stress response + CUMS, n=10), and an ABA-treated group (40 mg/kg/day ABA + are still not well understood. CUMS, n=12). Briefly, after one week of stress, the CUMS-treated Here, we propose that ABA may be a candidate for the nega- rats received fluoxetine, ABA, or vehicle on days 8–21; the con- tive regulation of CRH mRNA expression, and that ABA/RA is trol rats were administered an undisrupted vehicle treatment. a pair of CRH regulators involved in the regulation of HPA axis After the CUMS, depression behaviors were evaluated using the activity. Furthermore, ABA may share the capacity to regulate the sucrose intake, the open field test, and the forced swim test. All transcriptional expression of CRH with the RA signaling pathway. behavioral tests and the drug administration were performed in a soundproof room with a neutral environment between 0800 and 1400 h. Methods Animals and Drugs Tissue Preparation All Sprague Dawley (SD) rats were male and maintained with Blood samples were collected and centrifuged at 4°C (4 000 rpm, free access to food and water on a 12 h light/dark cycle (lights 10 min). Subsequently, the serum was separated for the deter- on 0700 h) at a room temperature of 22 ± 1◦C with 50–60% rela- mination of corticosterone (Corticosterone EIA Kit, Enzo Life tive humidity.
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