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Geniposide Alleviates Depression-Like Behavior Via Enhancing BDNF Expression in Hippocampus of Streptozotocin-Evoked Mice

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Geniposide Alleviates Depression-Like Behavior Via Enhancing BDNF Expression in Hippocampus of Streptozotocin-Evoked Mice Metab Brain Dis DOI 10.1007/s11011-016-9856-4 ORIGINAL ARTICLE Geniposide alleviates depression-like behavior via enhancing BDNF expression in hippocampus of streptozotocin-evoked mice Junming Wang1,2 & Peili Duan 2 & Ying Cui1,2 & Qing Li2 & Yanran Shi 2 Received: 4 February 2016 /Accepted: 9 June 2016 # Springer Science+Business Media New York 2016 Abstract Clinical and preclinical data suggest that diabetes is indicate that GP can alleviate depression-like behavior in often psychological complications such as depression. STZ-evoked diabetic mice, and suggest its mechanisms may Geniposide (GP), a major compound in Gardenia jasminoides partially be ascribed to up-regulating BDNF expression in Ellis with both medicinal and nutritional values, has been brain. previously confirmed to exert anti-diabetic and anti- depressive activities. The present study attempted to observe Keywords Antidepressant . Geniposide . Brain-derived anti-depressive mechanisms of GP in streptozotocin (STZ) neurotrophic factor . Diabetic complications . Forced evoked diabetic mice by involving brain-derived neurotrophic swimming test factor (BDNF), for the first time. Mice were given GP daily (50, and 100 mg/kg, ig) or reference drugs FHMH [fluoxetine hydrochloride (FH, 10 mg/kg, ig)combinedwithmetformin Introduction hydrochloride (MH, 100 mg/kg, ig)] for 3 weeks. The forced swimming test (FST) was performed to observe depression- Diabetes mellitus (DM) is one of the most commonly occur- like behavior, and serum and brain tissues were used for neu- ring chronic diseases with recent estimates suggesting 366 rochemical and fluorescent quantitative reverse transcription million people currently affected (Rhee 2015). DM is often PCR analyses. STZ induced excessively increased blood sug- associated with psychological complications such as depres- ar and immobility time in FST, in a manner attenuated by GP sion, which have severe impact on morbidity and mortality and FHMH administration. GP administration further elevated (Islam et al. 2015). A literature review has shown that about BDNF levels, and up-regulated the mRNA expression of 42 % of patients with diabetes have elevated levels of depres- BDNF and tropomyosin-related kinase B (TrkB) in hippo- sion symptoms (Gemeay et al. 2015). In addition, recent clin- campus of diabetic mice. In addition, STZ induced the exces- ical studies have shown the prevalence of depression in dia- sive level of serum corticosterone (CORT), while GP did not betic patients is much higher than the normal population influence on it in diabetic mice. Taken together, these findings (Zhang et al. 2015a, 2015b, 2015c), supporting the notion that there exists a strong link between diabetes and depression disorder. Coexisting depression in people with diabetes causes significantly decreased adherence to treatment, poor metabol- * Junming Wang [email protected] ic control, higher complication rates, decreased quality of life, increased healthcare use and cost, increased disability and lost productivity, and increased risk of death (Egede and Ellis 1 Collaborative Innovation Center for Respiratory Disease Diagnosis 2010). Depression in patients with diabetes is associated with and Treatment & Chinese Medicine Development of Henan Province, Henan University of Traditional Chinese Medicine, less frequent blood glucose monitoring and suboptimal glyce- Zhengzhou 450046, China mic control (Gemeay et al. 2015), which further worse the 2 College of Pharmacy, Henan University of Traditional Chinese diabetic condition. Medicine, East Jinshui Road & Boxue Road, Zhengzhou 450046, Streptozotocin- (STZ-) evoked diabetes is among the most China widely used preclinical models. Previous reports have shown Metab Brain Dis that STZ-induced diabetes results in depression-like behavior antioxidative enzyme heme oxygenase-1 (HO-1) (Yin et al. in various preclinical testing paradigms (Castillo-Gómez et al. 2010a), antidepressant-like effect on chronic unpredictable 2015). STZ-induced diabetes has demonstrated significantly mild stress-induced depressive rats by regulating the prolonged immobility time in tail suspension and forced hypothalamus-pituitary-adrenal axis (Cai et al. 2015)and swimming tests which are both the important behavioral tests anti-diabeticeffect(Yaoetal.2014), etc. However, as for its with strong predictive validity (Anjaneyulu et al. 2003;Kamei antidepressant-like effect on diabetes, there is no experimental et al. 2003). report until now. Furthermore, whether its mechanism is asso- Increasing evidence suggests that brain-derived neuro- ciated with BDNF has not been known. trophic factor (BDNF), as one of the neurotrophin families The present study was designed to assess the of growth factors with an important impact on the survival antidepressant-like effect of GP on STZ-evoked diabetic mice and synaptic of neurons in the adult central nervous system and the mechanism involved in BDNF by means of behavioral (CNS), may play important roles in the pathogenesis of dia- and pharmacological procedures. betes as well as depression, and contribute to the association of diabetes and depression (Alzoubi et al. 2013; Caletti et al. 2015; El-Marasy et al. 2014; Lenart et al. 2016; Wang and He Materials and methods 2015;Wangetal.2012;Zhouetal.2013). On the one hand, both animal and clinical experiments showed that BDNF has Experimental animals important influence on the pathobiology of diabetes, because BDNF modulates the secretion and actions of insulin, leptin, Male Kunming (KM) male mice (18–22 g) were purchased ghrelin, various neurotransmitters and peptides, and pro- from Experimental Animal Center of Henan Province inflammatory cytokines related to energy homeostasis (Rao (Zhengzhou, Henan Province, China). Animals were given et al. 2008). On the other hand, a strong association between rodent laboratory chow and water ad libitum, and maintained BDNF and depression has been demonstrated in both clinical under controlled conditions with a temperature of 22 ± 1 °C, and animal studies. For instance, animal experiments have relative humidity 60 ± 10 % and a 12/12 h light/dark cycle showed that BDNF decrease was associated with depressive (lights on at 7:00 a.m.). All the procedures were in strict ac- states, and clinical investigations revealed that BDNF levels in cordance with the P.R. China legislation on the use and care of depressed patients were lower than those in normal controls laboratory animals and with the guidelines established by and supplementary BDNF was able to reverse depressive sta- Institute for Experimental Animals of Henan University of tus (Haghighi et al. 2013;Lietal.2016). BDNF may play an Traditional Chinese Medicine and were approved by the uni- important role in the pathogenesis of depression and, there- versity committee for animal experiments. fore, might participate in the therapeutic actions of antidepres- sants (Kerman 2012). Reagents Geniposide (GP), an iridoid glycoside isolated from the Chinese herb Gardenia jasminoides (Zhizi), possesses diverse Geniposide (GP) was provided from Shanghai Jinsui bioactivities including neuroprotection in the MPTP mouse Biotechnology Co., Ltd. (Shanghai, China) with the purity model of Parkinson’s disease by enhancing growth factor sig- more than 98 % as assayed by high-performance liquid chro- naling and the reduction of apoptosis (Chen et al. 2015), ame- matography (HPLC). Fluoxetine hydrochloride (FH) was pur- liorating cerebral ischemia-reperfusion injury in rats by the chased from Changzhou Siyao Pharmaceuticals Co., Ltd. enhancement of BDNF and inhibition of caspase-3 (Zhang (Changzhou, Jiangsu Province, China). Metformin hydro- et al. 2006a; b), ameliorating learning memory deficits, reduc- chloride (MH) was purchased from Shanghai Xinyi ing tau phosphorylation and decreasing apoptosis via GSK3β Pharmaceuticals Co., Ltd. (Shanghai, China). Streptozotocin pathway in streptozotocin-induced alzheimer rat model (Gao (STZ), purchased from Sigma Chemical Co. (St. Louis, et al. 2014), attenuating insulin-deficiency-induced accelera- Missouri, USA), was dissolved in sodium citrate buffer tion of β-amyloidosis in an APP/PS1 transgenic model of (0.1 mol/L, pH 4.2) immediately before its administration. Alzheimer’s disease via enhancing insulin signaling (Zhang Mouse corticosterone (CORT) and BDNF enzyme-linked im- et al. 2015a, 2015b, 2015c), protecting human neuroblastoma munoassay (ELISA) kits (R&D system) were purchased from cells (SH-SY5Y cell line) against formaldehyde stress through R&D Systems China Co. Ltd. (Shanghai, China). modulating the expression of Bcl-2, P53, caspase 3 and cas- pase 9, and by increasing the activity of intracellular superox- Diabetes induction ide dismutase and glutathione peroxidase (Sun et al. 2013), antagonizing oxidative stress probably involving phos- Experimental diabetes was induced following an overnight phatidylinositol 3′-kinase (PI3K)- and nuclear factor-E2- fast by a single intraperitoneal (ip) injection of STZ at the dose related factor 2 (Nrf2)-mediated upregulation of the of 60 mg/kg freshly dissolved in sodium citrate buffer (0.1 M, Metab Brain Dis pH 4.2). Hyperglycemia was confirmed 72 h after STZ ad- Assay for Open Field Test (OFT) ministration by a portable Freestyle glucometer (Jiangsu Yuyue Medical Equipment & Supply Co. Ltd., Danyang, Locomotor activity was observed by the open field test (OFT) Jiangsu Province, China) in a blood sample obtained by tail through a modified method (Porsolt et al. 1977). Briefly, the prick
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