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Antiplatelet Activity of Obovatol, a Biphenolic Component of Magnolia Obovata, in Rat Arterial Thrombosis and Rabbit Platelet Aggregation

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Antiplatelet Activity of Obovatol, a Biphenolic Component of Magnolia Obovata, in Rat Arterial Thrombosis and Rabbit Platelet Aggregation Journal of Atherosclerosis and Thrombosis Vol.18, No.8 659 Original Article Antiplatelet Activity of Obovatol, a Biphenolic Component of Magnolia Obovata, in Rat Arterial Thrombosis and Rabbit Platelet Aggregation Eun-Seok Park1, Yong Lim2, Seung-Ho Lee1, Byoung-Mog Kwon3, Hwan-Soo Yoo1, Jin-Tae Hong1, 4, and Yeo-Pyo Yun1 1College of Pharmacy, Chungbuk National University, Cheongju, Republic of Korea 2Department of Clinical laboratory Science, Dong-eui University, Busan, Republic of Korea 3Laboratory of Chemical Biology and Genomics, Korea Research Institute of Bioscience and Biotechnology, Daejeon, Republic of Korea 4College of Pharmacy, Medical Research Center, Chungbuk National University, Cheongju, Republic of Korea Aim: Thrombosis occurs in the coronary arteries via the activation of platelets, and leads to acute myocardial infarction and sudden death. Obovatol, a major biphenolic component of Magnolia obo- vata leaves, displays anti-inflammatory and acyl Co-A cholesterol acyltrasferase inhibitory effects. The purpose of this study was to determine the effects of obovatol on thrombus formation in vivo and platelet activation in vitro and ex vivo. Methods: We investigated the antiplatelet and antithrombotic activities of obovatol in rat carotid ar- terial thrombosis in vivo along with platelet aggregation in vitro and ex vivo. Its possible cellular mechanism of antiplatelet activity was investigated by testing PLC-γ2 activation, arachidonic acid cascade, calcium mobilization and granule secretion. Results: Oral administration of obovatol prevented carotid thrombosis, but also significantly inhibit- ed collagen-induced platelet aggregation. Obovatol did not change coagulation times, such as activat- ed partial thromboplastin time and prothrombin time, indicating that the antithrombotic effect of obovatol might be due to antiplatelet activity rather than anticoagulation activity. Obovatol inhibited in vitro collagen- and arachidonic acid-induced rabbit platelet aggregation in a concentration-depen- dent manner (1-10 μM), with IC50 values of 2.4±0.8 and 4.8±0.9 μM, respectively. Obovatol blocked collagen-mediated phospholipase C-γ2 phosphorylation, cytoplasmic calcium mobilization, arachidonic acid liberation and serotonin secretion. Conclusion: Obovatol has a potent antithrombotic effect, which may be due to antiplatelet activity. The antiplatelet activity of obovatol is mediated by inhibition of PLC-γ2 phosphorylation. Thus, obovatol may be a potential candidate to treat cardiovascular disease. J Atheroscler Thromb, 2011; 18:659-669. Key words; Obovatol, Antiplatelet activity, PLC-γ2, Thrombosis, FeCl3-induced thrombosis model array of ligands, such as collagen, von Willebrand fac- Introduction tor (vWF), ADP and thrombin, are generated at the Once blood vessels become damaged, a diverse injury site and induce platelet adhesion, followed by activation and aggregation1). Collagen enhances the Address for correspondence: Yeo-Pyo Yun, College of Pharmacy, adhesion of platelets to the injury site and induces Chungbuk National University, 48 Gaeshin-Dong, Heungduk- Gu, Cheongju, 361-763, Korea platelet activation through a tyrosine kinase-based sig- E-mail: [email protected] naling pathway. Collagen activates the kinase Syk and Received: October 24, 2010 phospholipase C-γ2 (PLC-γ2), and leads to increased Accepted for publication: February 15, 2011 cytoplasmic calcium, shape change and granule re- 660 Park et al. Antiplatelet Activity of Obovatol 661 lease2-5). Collagen-induced platelet activation results in tional University, Korea. platelet shape change and the release of substances that recruit activated platelets to the developing Arterial thrombus formation in vivo 6, 7) thrombus . The rat FeCl3 thrombosis model used for these When various inducers activate platelets, arachi- studies was modified from that described19). Obovatol donic acid is increased markedly via PLA2-mediated was orally administered to male Sprague-Dawley rats phospholipid hydrolysis8, 9). There are two main path- (240-260 g) daily at doses of 50 and 100 mg/kg for 3 ways of arachidonic acid metabolism in platelets. One days or carboxymethylcellulose (CMC) as a vehicle. is the cyclooxygenase (COX) pathway, which produc- The rats were anaesthetized with pentobarbital sodi- es TXA2; the other is the 12-lipoxygenase (12-LOX) um salt (60 mg/kg, intraperitoneally). A segment of pathway, which produces 12-hydroxy-eicosatetraenoic the right carotid artery was exposed and dissected free acid (12-HETE). 12-HETE plays a positive feedback of the vagus nerve and surrounding tissues and then role in thrombus formation in vivo10) and gives rise to fitted on the Doppler flow probe (1 mm diameter). platelet aggregation and aortic smooth muscle cell mi- Blood flow was measured with a Doppler velocimeter 11, 12) gration in vitro . 12-HETE and TXA2 appear to (Crystal Biotech, Hopkinton, MA, USA). After be involved in the initiation and propagation of 60-min administration of obovatol, thrombus was in- thrombotic and atherosclerotic disorders. Although duced by placing a 2-mm2 Whatman no. 1 filter pa- various arachidonic acid metabolites are produced per saturated with 50% ferric chloride (FeCl3) on the from COX and LOX, TXA2 and 12-HETE activities carotid artery near the probe for 10 min. The time play a major role in thrombosis13). needed for occlusion to occur was measured for up to Magnolia (Hou Po) was used medicinally as early 60 min, and the occlusion time was assigned as a val- as the first century and is a commonly prescribed Chi- ue of 60 min for vessels that did not occlude within nese traditional medicine. It possesses antioxidant ac- 60 min. tivity approximately 1000 times greater than α-to- copherol14). The biphenolic components from Magno- Platelet aggregation and coagulation times assay ex lia obovata, including magnolol, honokiol and obova- vivo tol, exhibit antiplatelet15), antitumor16) and antiin- Male Sprague-Dawley rats (240-260 g) were oral- flammatory activities17, 18). In our ongoing search for ly administered obovatol (50 and 100 mg/kg) for 3 antiplatelet agents from natural resources, we found days or CMC as a vehicle, and then blood was collect- that obovatol exhibited potent antiplatelet activity. In ed and platelet-rich plasma (PRP) was prepared by the study, we investigated the antiplatelet activity of centrifuging the blood sample at 180 ×g for 10 min obovatol by measuring in vitro and ex vivo agonist-in- and platelet-poor plasma (PPP) was obtained by cen- duced platelet aggregation. Its possible cellular mecha- trifuging the PRP at 2100 ×g for 10 min. PRP was nism of antiplatelet activity was investigated by testing adjusted to a density of 3×108 platelets/ml with PPP. PLC-γ2 activation, arachidonic acid cascade, calcium Platelet aggregation was measured as previously de- mobilization and granule secretion. We also evaluated scribed20) using an aggregometer (Chrono-Log Co., the antithrombotic activity of obovatol in the ferric Havertown, PA, USA). ADP (2 μM) and collagen (10 chloride-induced arterial thrombosis model in rats. μg/ml) were used as agonists for platelet aggregation. Anticoagulation activity was evaluated by measuring plasma-clotting times. The plasma activated partial Materials and Methods thromboplastin times (APTT) and prothrombin times Experimental animals (PT) were automatically measured using an Automat- Male Sprague-Dawley rats were purchased from ed Coagulation Laboratory 100 Instrument (Instru- Dae-Han Biolink Co. (Eum sung, Korea) and accli- mentation Laboratory Co., Milano, Italy). mated for 1 week at 24±1 ℃ and 55±5% humidity. Male New Zealand white rabbits (n =8) were pur- Measurement of washed rabbit platelet preparation chased from SamTako Bio Korea Inc. (Osan, Korea) and aggregation and acclimated for at least 1 week at 24±1 ℃ and 55 Rabbits were fixed in a cage. Blood was drawn ±5% humidity, with free access to drinking water and from the ear artery of conscious rabbits and collected a commercial pellet diet obtained from SamTako Bio directly into Vacutainer tubes containing anticoagu- Korea Inc. before experiments. Animal experiments lant solution (composed of 0.8% citric acid, 2.2% tri- were carried out in accordance with the Guide for the sodium citrate, and 2% dextrose (w/v)). PRP was pre- Care and Use of Laboratory Animals, Chungbuk Na- pared by centrifugation at 230 ×g for 10 min at room 660 Park et al. Antiplatelet Activity of Obovatol 661 temperature. Platelets were sedimented by centrifuga- samples were then centrifuged at 2100 ×g at 4℃ for tion of PRP at 2100 ×g for 10 min and then washed 10 min, and the upper phase was removed and evapo- twice with HEPES buffer (137 mM NaCl, 2.7 mM rated to dryness under nitrogen. Residues were dis- KCl, 1 mM MgCl2, 5.6 mM glucose, 0.35% bovine solved in chloroform/methanol (2:1, v/v) and applied serum albumin, and 3.8 mM HEPES, pH 6.5) con- to thin layer chromatography plates. The plates were taining 0.4 mM EGTA. After centrifugation, the pel- developed in petroleum ether/diethyl ether/acetic acid lets were resuspended in HEPES buffer (pH 7.4). The (40:40:1, v/v/v). The area corresponding to arachi- platelet concentration was counted using a Coulter donic acid or diacylglycerol was scraped off, and ra- Counter (Coulter Electronics, Hialeah, FL, USA) and dioactivity was determined. adjusted to 4×108 platelets per milliliter. Platelet ag- gregation was measured as previously described20). Measurement of serotonin secretion Briefly, washed platelet suspensions
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