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Isochaihulactone Protects PC12 Cell Against H2O2 Induced Oxidative Stress and Exerts the Potent Anti- Aging Effects in D-Galactose Aging Mouse Model

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Isochaihulactone Protects PC12 Cell Against H2O2 Induced Oxidative Stress and Exerts the Potent Anti- Aging Effects in D-Galactose Aging Mouse Model npg Acta Pharmacologica Sinica (2010) 31: 1532–1540 © 2010 CPS and SIMM All rights reserved 1671-4083/10 $32.00 www.nature.com/aps Original Article Isochaihulactone protects PC12 cell against H2O2 induced oxidative stress and exerts the potent anti- aging effects in D-galactose aging mouse model Sung-liang YU1, #, Shih-bin LIN2, 4, #, Yung-luen YU3, #, Min-hui CHIEN4, Kuo-jung SU4, Ching-ju LIN4, Tzong-der WAY5, Giou- teng YIANG6, Chai-ching LIN4, 7, De-chuan CHAN8, Horng-jyh HARN9, Yi-lin Sophia CHEN4, * 1Department of Clinical Laboratory Science and Medical Biotechnology, College of Medicine National Taiwan University, Taipei, Taiwan, China; 2Department of Food Science, National Ilan University, Ilan, Taiwan, China; 3Graduate Institute of Cancer Biology and Center for Molecular Medicine, China Medical University and Hospital, Taiwan, China; 4Graduate Institute of biotechnology, National Ilan University, Ilan, Taiwan, China; 5Department of Biological Science and Technology, College of Life Sciences, China Medical University, Taichung, Taiwan, China; 6Department of Emergent Medicine, Buddhist Tzu Chi University and General Hospital, Hualien and Taipei Branch, Hualien, Taiwan, China; 7Department of Animal Science, National Ilan University, Ilan, Taiwan, China; 8Division of General Surgery, Department of Surgery, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan, China; 9Department of Pathology, China Medical University and Hospital, Taichung, Taiwan, China Aim: To investigate the effect of isochaihulactone (also known as K8), a lignan compound of Bupleurum scorzonerifolium, on H2O2- induced cytotoxicity in neuronally differentiated PC12 cells (nPC12). Methods: Viability of neuronal PC12 cells was measured using MTT assay. Protein expression was determined by Western blot. Apop- totic cells was determined using TUNEL assay. D-galactose aging mice were used as a model system to study the anti-oxidant effects of isochaihulactone in vivo. Results: Pretreatment with isochaihulactone (5–10 μmol/L) increased cell viability and decreased membrane damage, generation of reactive oxygen species and degradation of poly (ADP-ribose) polymerase in H2O2-treated nPC12 cells and also decreased the expres- sion of cyclooxygenase-2, via downregulation of NF-kappaB, resulting in a decrease in lipid peroxidation. The results suggest that isochaihulactone is a potential antioxidant agent. In a murine aging model, in which chronic systemic exposure to D-galactose (D-gal) causes the acceleration of senescence, administration of isochaihulactone (10 mg·kg-1·d-1, sc) for 7 weeks concomitant with D-gal injection significantly increased superoxide dismutase and glutathione peroxidase activities and decreased the MDA level in plasma. Furthermore, H&E staining to quantify cell death within hippocampus showed that percentage of pyknotic nuclei in the D-gal-treated mice were much higher than in control. Conclusion: The results suggest that isochaihulactone exerts potent anti-aging effects against D-gal in mice possibly via antioxidative mechanisms. Keywords: lignan; isochaihulactone; neuroprotection; cyclooxygenase-2; anti-aging; PC12 cells; D-galactose; aging Acta Pharmacologica Sinica (2010) 31: 1532–1540; doi: 10.1038/aps.2010.152; published online 1 Nov 2010 Introduction sis[4–6]. Superoxide dismutase (SOD), catalase (CAT) and glu- Oxidative stress is believed to be a primary factor in neu- tathione peroxidase (GPx) act by scavenging the superoxide rodegenerative diseases as well as in the normal process of anion and H2O2 to prevent reactive oxygen species (ROS)- [1–3] [7] aging . Oxygen-derived free radicals exert detrimental induced damage . Exogenous H2O2 can increase oxidative effects including peroxidation of membrane lipids, enzyme stress and apoptotic cell death by causing mitochondrial dys- inactivation, DNA fragmentation and activation of apopto- function and activation of caspases. Therefore, H2O2 has been used extensively as an inducer of oxidative stress in in vitro models. # These authors contributed equally to the work. * To whom correspondence should be addressed. Reactive oxygen species themselves can increase and/or [8–10] E-mail [email protected] induce cellular cyclooxygenase-2 (COX-2) expression . In Received 2010-05-17 Accepted 2010-08-02 addition, apoptotic cell death induced by exposure to cyanide www.chinaphar.com npg Yu SL et al 1533 [11, 12] can be inhibited by selective COX-2 inhibition . Oxidative 1635, 1581, 1335, 1153; UV (CHCl3) lmax nm (log e): 247 (4.08), 1 stress-induced COX-2 expression can be prevented in numer- 298 (4.17), 327 (4.08); H NMR (CDCl3) d: 3.29 (1H, m, H-3), ous cell types, including neurons, by free radical scavengers. 4.10 (1H, dd, J=9.0, 3.8 Hz, H-4a), 4.31 (1H, dd, J=9.0, 7.3 Hz, Thus, oxidant stressors are specific and important inducers of H-4b), 6.60 (1H, d, J=1.5 Hz, H-5), 2.78 (1H, dd, J=13.7, 9.0 Hz, COX-2 gene expression. H-6a), 2.92 (1H, dd, J=13.7, 6.7 Hz, H-6b), 7.24s (2H, s, H-20, The free radical theory of aging was conceived by Harman 60), 6.67 (1H, d, J=1.4 Hz, H-200), 6.74 (1H, d, J=7.8 Hz, H-500), in 1956. Increasing evidence has convinced many researchers 6.61 (1H, dd, J=7.8, 1.4 Hz, H-600), 3.87 (9H, s, OMe), 5.93 (1H, 13 that oxidants play an important role in aging. Chronic admin- d, J=1.3 Hz, OCH2O), 5.94 (1H, d, J=1.3 Hz, OCH2O); C NMR istration of a low dose of D-galactose (D-gal) induces changes (CDCl3) d: 169.29s (C-1), 126.36s (C-2), 44.43d (C-3), 69.82t that resemble natural aging in animals[13–20]. D-galactose is (C-4), 140.60d (C-5), 40.72t (C-6), 128.83s (C-10), 108.65d (C-20), a physiological nutrient obtains from lactose in milk. The 152.62s (C-30), 139.61s (C-40), 152.62s (C-50), 108.65d (C-60), hydrolysis of lactose in the intestine results monosaccharide 131.31s (C-100), 109.29d (C-200), 147.94s (C-300), 146.49s glucose and galactose. In animals, galactose is normally (C-400), 108.39d (C-500), 122.29d (C-600), 56.18q (20-OMe), metabolized by D-galactokinase and galactose-1-phosphate 60.90q (30-OMe), 56.18q (40-OMe), 101.03t (OCH2O); EIMS, 70 uridyltransferase but over-supply of D-galactose results its eV, m/z (rel int): 398 ([M]+, 18), 263 (100), 207 (16), 135 (35). abnormal metabolism (Kaplan and Pesce, 1996). D-galactose was converted into galactitol, which is not metabolized Chemicals and reagents by above enzymes but accumulate in the cell, that leads to Isochaihulactone was dissolved in DMSO to a concentra- osmotic stress and ROS production[21]. In addition, supple- tion of 100 mmol/L and stored in -20 °C as a stock solution. mentation with antioxidants has been reported to be beneficial Dimethyl sulfoxide (DMSO), 3-(4,5-dimethyl thizol-2-yl)-2,5- with respect to slowing the aging process[22, 23]. diphenyl tetrazolium bromide (MTT), 2’,7’-dichlorofluorescein Nan-Chai-Hu (Chai Hu of the South), the root of Bupleurum diacetate (H2DCF-DA), Hoechst 33342, thiobarbituric acid [24] scorzonerifolium, is an important Chinese herb . Isochaihu- (TBA), hydrogen peroxide (H2O2), trichloroacetic acid (TCA), lactone (also known as K8) is a lignan compound that was malondialdehyde (MDA), propidium iodine (PI) and actin identified in acetone extracts of Nan-Chai-Hu and shows anti- antibody were purchased from Sigma Chemical Co (St Louis, tumor activity against A549 cells in vitro and in vivo[25, 26]. Lig- MO, USA). F-12 medium, horse serum, fetal bovine serum nan compounds (eg, sesamin, sesamolin) have been reported (FBS), penicillin, streptomycin, trypsin/EDTA and NuPAGE to act as neuroprotective agents against oxidative injury and Bis-Tris Electrophoresis System (pre-cast polyacrylamide mini- excitotoxicity[27–30]. Lignans can also inhibit lipopolysaccha- gel) were purchased from Invitrogen (Carlsbad, CA, USA). ride-inducible COX-2 expression in macrophages[31]. The aim CellBIND surface dishes and mouse 2.5S nerve growth factor of the present study was to investigate the effects of isochaihu- (NGF) were purchased from Millipore (Bedford, MA). COX-2 lactone on H2O2-induced injury in neuronal PC12 cells (nPC12) antibody was purchased from Thermo scientific (Waltham, and in a murine D-gal–induced aging model. MA, USA). PARP antibodies and horseradish peroxidase- conjugated anti-mouse or anti-rabbit IgG secondary antibodies Materials and methods were purchased from Cell signaling (MA, USA). Polyvinyldi- Fraction purification of isochaihulactone and structure fluoride (PVDF) membranes, BSA protein assay kit and West- determination ern blot chemiluminescence reagent were purchased from B scorzonerifolium roots were supplied from Chung-Yuan Co, Amersham Biosciences (Arlington Heights, IL). Superoxide Taipei, and the plant was identified by Professor Lin of the dismutase activity assay kit was purchased from BioVision National Defense Medicinal Center, where a voucher speci- (Mountain View, CA). Glutathione peroxidase assay kit was men was deposited (NDMCP No 900801). The acetone extract purchased from Cayman Chemical (MI, USA). DNA Frag- AE-BS was prepared as described previously[25, 32]. The AE-BS mentation Assay Kit was purchased from Clontech Laborato- was dissolved in 95% MeOH solution and then partitioned ries (Mountain View, CA). Non-Radioactive Cytoxicity Assay (1:1) with n-hexane to give the n-hexane-soluble fraction Kit was purchased from promega (Madison, WI, USA). (BS-HE). The aqueous 95% MeOH layer was evaporated to remove residual MeOH, and then distilled water was added. Cell culture and differentiation of neuronal PC12 cells This aqueous solution was further partitioned with CHCl3 to Undifferentiated rat phenchromocytoma cells (PC12 cells) get the CHCl3-soluble fraction (BS-CE) and H2O-soluble frac- were obtained from the Bioresources Collection and Research tion (BS-WE). The BS-CE was subjected to chromatography Center (BCRC, Hsin Chu, Taiwan) and maintained in F-12 over silica gel and eluted with CH2Cl2, CH2Cl2-MeOH (95:5), medium supplemented with 2.5% fetal bovine serum and CH2Cl2-MeOH (9:1), CH2Cl2-MeOH (8:2) and MeOH, succes- 12.5% horse serum in a CO2 incubator at 37 °C.
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