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Daidzein Activates Choline Acetyltransferase from MC-IXC Cells and Improves Drug-Induced Amnesia

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Daidzein Activates Choline Acetyltransferase from MC-IXC Cells and Improves Drug-Induced Amnesia Biosci. Biotechnol. Biochem., 70 (1), 107–111, 2006 Daidzein Activates Choline Acetyltransferase from MC-IXC Cells and Improves Drug-Induced Amnesia Ho Jin HEO,1;2 Young-Min SUH,2 Mi-Jeong KIM,2 Soo-Jung CHOI,2 Nam Shik MUN,3 Hye-Kyung KIM,4 Eunki KIM,5 Chang-Ju KIM,6 y Hong-Yon CHO,2 Young Jun KIM,2 and Dong-Hoon SHIN2; 1Jeonnam Innovation Agency, #100 Namak-ri, Samhyang-myeon, Muan-county, Jeonnam 534-700, Korea 2Graduate School of Biotechnology, Korea University, Seoul 136-701, Korea 3Department of Psychiatry, College of Medicine, Chosun University, Gwangju 501-759, Korea 4Department of Food Biotechnology, Hanseo University, Seosan 356-706, Korea 5Department of Biological Engineering, Inha University, Incheon 402-751, Korea 6Department of Physiology, Kyung Hee University, Seoul 130-701, Korea Received June 21, 2005; Accepted October 14, 2005 The choline acetyltransferase (ChAT) activator, is known to be related both to the degree of dementia which enhances cholinergic transmission via an aug- and to the severity of the neuropathological hallmarks of mentation of the enzymatic production of acetylcholine AD. ChAT activity was significantly lower in AD (ACh), is an important factor in the treatment of patients than in age-matched control subjects in the Alzheimer’s disease (AD). Methanolic extracts from frontal cortex, temporal cortex, hippocampus, and Pueraria thunbergiana exhibited an activation effect cerebellum.1) The most consistent biochemical finding (46%) on ChAT in vitro. Via the sequential isolation of in AD patients is a decrease in ACh levels within the Pueraria thunbergiana, the active component was ulti- basal forebrain.2) This enzyme is a single-strand globular mately identified as daidzein (40,7-dihydroxy-isofla- protein, which is synthesized in the perikarion and then vone). In order to investigate the effects of daidzein transported to the nerve terminals, probably via both from Pueraria thunbergiana on scopolamine-induced slow and rapid axoplasmic flow.3) ChAT is known to be impairments of learning and memory, we conducted present in abundance in the cytosol of the cholinergic a series of in vivo tests. Administration of daidzein cell bodies. Approximately 80–90% of the ChAT (4.5 mg/kg body weight) to mice was shown significantly located in the nerve terminals exists as a cytosolic to reverse scopolamine-induced amnesia, according to protein, a portion of which may be ionically associated the results of a Y-maze test. Injections of scopolamine with the synaptic membranes, whereas the remaining into mice resulted in impaired performance on Y-maze 10–20% of the total enzyme appears to be nonionically tests (a 37% decreases in alternation behavior). By way bound to the plasma membrane.4) Despite the key role of of contrast, mice treated with daidzein prior to the ChAT in neurotransmission, the extremely low amounts scopolamine injections were noticeably protected from and instability of the enzyme in the nervous tissues are this performance impairment (an approximately 12%– factors that hinder biochemical and structural analysis.5) 21% decrease in alternation behavior). These results One strategy aimed toward the amelioration of AD indicate that daidzein might play a role in acetylcholine symptoms is the restitution of near-normal acetylcholine biosynthesis as a ChAT activator, and that it also concentrations in the synaptic cleft, which might ameliorates scopolamine-induced amnesia. improve cholinergic neurotransmission. ChAT activa- tors have been shown to effect an increase in ACh Key words: amnesia; choline acetyltransferase; daidzein synthesis, elevating the endogenous ACh levels in the brain and thereby enhancing cholinergic neurotransmis- The etiological events that lead to Alzheimer’s sion, resulting in an improvement of cognitive function disease (AD) remain somewhat obscure, but highly in cases of mild to moderate AD. In an attempt to typical neuropathological changes have been observed identify a natural active constituent which can signifi- in the brains of AD patients. A reduction in choline cantly increase ChAT levels, we screened 90 Korean acetyltransferase (ChAT, EC 2.3.1.6), a synthetic en- traditional tea plants. We identified a daidzein (40,7- zyme of acetylcholine (ACh) in the cholinergic neurons, dihydroxy isoflavone) of Pueraria thunbergiana,a y To whom correspondence should be addressed. Tel: + 82-2-923-8732; Fax: +82-2-3290-3429; E-mail: [email protected] Abbreviations: AD, Alzheimer’s disease; ACh, acetylcholine; AChE, acetylcholinesterase; ChAT, choline acetyltransferase; SCOP, scopolamine 108 H. J. HEO et al. member of the Leguminosae family. We then assessed (22–24), 20:80 (25–27), 10:90 (28–30), 0:100 (31–33); daidzein’s possible effects with regard to the reversal or v/v] respectively (flow rate, 2.5 ml/min). The activation amelioration of scopolamine-induced learning and of enzyme activity for each of the fractions was memory deficits. calculated in comparison with the control values. The sample concentration was 500 mg/ml. The values repre- Materials and Methods sent the means ðn ¼ 3ÞSD. Thirty-three fractions were evaporated for tests. Among these, the no. 5 sub- Materials. The dried plants were purchased in a local fraction (90:10) activated ChAT to a level 80% over market for Oriental medicines in Seoul, Korea in 2000, control levels. The No. 5 sub-fraction was evaporated and were ground until the resulting powder could be to dryness (74 mg) under reduced pressure and dissolved passed through a fine screen (about 1 mm). The plant in chloroform (1 ml). It was then fractionated by a materials were authenticated by the Institute of Bio- second silica gel open column chromatography. It technology at Korea University, in which voucher was then subjected to a chromatographic open column specimens are maintained. Minimum Essential Medium (1:5 Â 30 cm) packed with silica gel suspended in (MEM), penicillin, and streptomycin were acquired chloroform. The column was then washed with 200 ml from Gibco BRL (Grand Island, NY, U.S.A.). Acetyl of chloroform and eluted with 10 ml of a chloroform– coenzyme A (acetyl-1-14C) was provided by NEN methanol mixture, in the following ratio: [100:0 (1–3), (Boston, MA, U.S.A.). All of the other chemicals used 96:4 (4–6), 92:8 (7–9), 90:10 (10–12), 88:12 (13–15), were purchased from the Sigma Chemical (St. Louis, 85:15 (16–18), 82:20 (19–21), 0:100 (22–24); v/v] MO, U.S.A.). respectively (flow rate, 1.0 ml/min). The degree to which enzyme activity had been activated for each Isolation of daidzein from Pueraria thunbergiana. We fraction was calculated in comparison with the control screened 90 Korean traditional tea plants in our search values. The sample concentration was 500 mg/ml. for a ChAT activator that can be obtained from natural Values represent the means ðn ¼ 3ÞSD. Among these resources. Among these edible tea plants, methanol 24 fractions, sub-fractions 16–17 (85:15) exerted a extracts from the powdered roots of Pueraria thun- substantial activating effect on ChAT activity, elevating bergiana (1 kg) exhibited the most profound effects on the activity level to more than 135% above control ChAT activity (Table 1). An evaporated methanol values. The active fraction was then purified via HPLC. extract of Pueraria thunbergiana was dissolved in The condition of HPLC for purification was equal to that distilled water (120 ml). This dissolved extract was of analytical HPLC. Analytical HPLC was conducted then partitioned with hexane (360 ml, Â3), chloroform with a Waters 2690 (C18 -bondapak reverse column: (360 ml, Â3) and ethyl acetate (360 ml, Â3), respective- 3:9 Â 300 mm, mobile phase, 80 min gradient of 0– ly, for 24 h. Each layer was then concentrated using a 100% methanol in water, flow rate, 1 ml/min, detector: rotary evaporator. The ethyl acetate fraction exhibited PDA; injection volume, 20 ml). We noted a single significant activity. It was evaporated to dryness (3.5 g) significant peak at 39 min. The data were collected over under reduced pressure, then dissolved in chloroform a range of 200–800 nm, and detection was conducted at (3 ml). The sample was added to a chromatographic 248 nm (Millennium Manager System Ver. 2.15; Wa- open column (3:0 Â 40 cm) packed with silica gel ters, Milford, MA, U.S.A.). The structure of the resulting suspended in chloroform. The column was then washed compound was then analyzed by means of an Avance with 200 ml of chloroform, and eluted with 100 ml of DRX-600 1H-NMR (Bruker, Billerica, MA, U.S.A.) for chloroform–methanol mixtures in the following ratios: chemical shift and electron impact mass spectrometry [100:0 (1–3), 90:10 (4–6), 80:20 (7–9), 70:30 (10–12), (EI-MS: Hewlett-Packard 5890-JMS AX505WA, Palo 60:40 (13–15), 50:50 (16–18), 40:60 (19–21), 30:70 Alto, CA). Cell culture. MC-IXC cells were cultured and main- Table 1. Effects of Extracts from Various Edible Plants on ChAT tained according to the previously described methods.6) Activity The cells, which were obtained from a human neuro- Edible tea plants used Activation effect blastoma, were grown in Minimum Essential Medium for screening on ChAT activity (%)Ã (MEM) containing 15% fetal bovine serum (FBS). The 1 a MC-IXC cells were grown in the presence of penicillin Pueraria thunbergiana 46.1 Pueraria thunbergiana1-1 52.0a (100 U/ml) and streptomycin (0.1 mg/ml) at 37 C, in an Citrus junos1 25.4a atmosphere containing 5% CO2. They were passaged Fiatoua villosa1 30.1a when the culture had achieved 80–90% confluence. The 1Extracts with methanol. 1-1Extracts with ethyl acetate. cells were dislodged from the surfaces of the culture ÃChAT activity (%): The percentage of enzyme activity values for each of dishes (100 mm) and then dispersed into a single-cell the samples was calculated in comparison with the control activity.
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