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Thymol Decreases Apoptosis and Carotid Inflammation Induced by Hypercholesterolemia Through a Discount in Oxidative Stress

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Thymol Decreases Apoptosis and Carotid Inflammation Induced by Hypercholesterolemia Through a Discount in Oxidative Stress http://www.cjmb.org Open Access Original Article Crescent Journal of Medical and Biological Sciences Vol. 4, No. 4, October 2017, 186–193 eISSN 2148-9696 Thymol decreases apoptosis and carotid inflammation induced by hypercholesterolemia through a discount in oxidative stress Roshanak Bayatmakoo1, Nadereh Rashtchizadeh2*, Parichehreh Yaghmaei1, Mehdi Farhoudi3, Pouran Karimi3 Abstract Objective: Atherosclerosis sclerosis is a chronic inflammatory disease that can lead to cardiovascular and cerebrovascular disorders that are generally along with hypercholesterolemia and oxidative stress. Various surveys have shown that thymol is a polyphenolic compound with anti-inflammatory and antioxidant properties. This study aimed to investigate the anti- inflammatory and antiapoptotic effects of thymol on carotid tissue of hypercholesterolemic rats. Materials and Methods: Forty male Wistar rats were randomly divided into 4 groups with 10 members each (n = 10): a control group with a normal diet (ND), a group with a high-cholesterol (2%) diet (HD), a group with a high-cholesterol diet combined with thymol (24 mg/kg HD + T), and a group with a thymol diet (T). After preparing serum from peripheral blood of rats, lipid measurements were obtained, including total cholesterol (TC), high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C), and triglycerides (TG), by using a colorimetric method; the levels of oxidized LDL (OxLDL) were obtained through enzyme-linked immunosorbent assay (ELISA). The activities of superoxide dismutase (SOD) and glutathione peroxidase (GPx) antioxidant enzymes, as well as the concentrations of malondialdehyde (MDA) and serum total antioxidant capacity (TAC), were determined with the use of colorimetric methods. The protein expressions of Bcl2 and cleaved caspase 3 and the phosphorylation of p38 mitogen-activated protein kinase (MAPK) in rat carotid tissue were determined by an immunoblotting method. Results: The rats fed with a high-cholesterol diet for 8 weeks increased TC and OxLDL in HD group compared with the ND group (P < 0.01; OxLDL HD vs ND (214.42 ± 17.46 vs 69.13 ± 9.92; P < 0.01); (229.39 ± 13.26 vs 67.89 ± 5-14 (215.58 ± 12.46 vs 229.35 ± 13.26; P < 0.05, OxLDL HD vs HD + T 105.53 ± 10.44; P < 0.01). Both of them were decreased with the intervention of thymol in the HD + T group compared with the HD group. The amount of phosphorylation of p38 (p-p38) and the protein expression of cleaved caspase 3 showed a significant increase in the HD group compared with the ND group (P < 0.01). In contrast, the expression of Bcl-2 in the high-cholesterol diet group decreased compared with the control group (P < 0.01). A comparison of the p-p38 and the protein expression of cleaved caspase 3 between the T + HD and the HD groups showed that in both cases, thymol caused a decrease (p<0.01), whereas Bcl-2 effected an increase (P < 0.05). Regarding the oxidant and antioxidant indices, thymol significantly decreased the MDA level and increased the total antioxidant content (P < 0.01). Conclusion: The results of this study indicate that thymol significantly decreases the expression of inflammatory and apoptotic proteins in carotid tissue. However, this decrease is probably not mediated by an effect on lipid metabolism because thymol decreases the total level of cholesterol but has no significant effect on the LDL-C level as the atherogenic index. In addition, thymol possibly exerts an antioxidant effect without the direct involvement of antioxidant enzymes. Keywords: Atherosclerosis, Bcl2 protein, Cholesterol, Cleaved caspase 3, p38 mitogen-activated protein kinase Introduction Hypercholesterolemia is directly and closely related to Oxygen molecules exposed to different radiation and atherosclerosis (2,3) and is characterized by increasing stress by taking an electron from other molecules, cause plasma concentrations of low-density lipoprotein (LDL), damage other molecules, cells and DNA. This activity can and triglycerides (TG). The accumulation of LDL in result in various diseases, including cancer, brain damage, the intima and their oxidation lead to the formation of and heart disease, such as atherosclerosis sclerosis, as well atherosclerotic plaques, which is one the most common as weakness of the immune system. The production of causes of clogged arteries, heart attacks and strokes, reactive oxygen species (ROS), even in normal conditions, and cardiovascular diseases (CVDs) (4-7). In fact, the is inevitable in metabolic pathways; however, the damage caused by atherosclerosis represents a wide range antioxidants available in the body and obtained in the diet of particular cellular and molecular responses that, as a neutralize the effects of ROS (1). whole, can be regarded as inflammatory diseases (5). The Received 19 September 2016, Accepted 22 March 2017, Available online 2 April 2017 1Department of Biology, Science and Research Branch, Islamic Azad University, Tehran, Iran. 2Biotechnology Research Center, Tabriz University of Medical Sciences, Tabriz, Iran. 3Neurosciences Research Center (NSRC), Tabriz University of Medical Sciences, Tabriz, Iran. *Corresponding Author: Nadereh Rashtchizadeh, Tel/Fax: +989141145493, Email: [email protected] Bayatmakoo et al oxidation of LDL by ROS leads to production of oxidized (22). Thymol directly refines free radicals and activates LDL (OxLDL), releasing phospholipids, peroxidation of physiologic defense mechanisms to exert its antioxidant lipids and proteins, and production of malondialdehyde activities (23,24). As a powerful antioxidant with the (MDA). ability to increase the serum total antioxidant capacity and Activation of endothelial cells is more in areas of vessel inhibit peroxidation, thymol can prevent the progression that are under the hemodynamic pressure. OxLDL is the of atherosclerosis (25). simulator of inflammatory reactions (5,8), which attracts Given the above-mentioned discussion, this study blood monocytes, and calls and reproduces macrophages aimed (a) to investigate the effect of thymol on (5,9,10). This oxidative stress leads to the consumption antioxidant, apoptotic, and inflammatory markers; and of the support recovery substance of the antioxidant (b) to investigate the possible mechanism of this effect system, decreasing the level of glutathione and the activity by considering changes in antioxidant responses or of antioxidant enzymes, such as glutathione peroxidase peripheral blood lipid levels. (GPx), catalase, and SOD. Increasing lipid peroxidation and/or decreasing antioxidant protection have been Materials and Methods observed in metabolic diseases and unhealthy lifestyles Animals and can cause endothelial dysfunction and atherosclerosis. Male Wistar rats were purchased from the animal Clinical trials have shown that increasing ROS decreases laboratory of the Pasteur Institute in Karaj, Iran. The antioxidant formation, especially in patients with coronary number of rats placed in each group was determined by artery disease (CAD) (11,12). The oxidative stress using the following formula (26): stimulates inflammatory reactions and plays an important N=(Z1-a+Z1-β)2(SD12+SD22) /(M1M2) role in the progression of atherosclerosis by launching the The criteria for inclusion in the study were a normal signaling (13,14). weight of about 270 ± 30 g, young age (8 weeks), good Protein of p38 mitogen-activated protein kinase health, male gender, and a normal lipid profile. The (MAPK) as an important pro-inflammatory marker exclusion criteria were presence of hyperlipidemia and controls cellular responses to stress and inflammation. behavioral abnormalities. For 1 week, the animals were Modified LDL, cytokines, and stressful events cause the kept at a temperature of 21°C, humidity of 55%, and phosphorylation and activation of p38 in endothelial cells a 12-hour light/dark cycle for them to get used to the and macrophages (15). environment (27), with access to sufficient food and water. The family of B-cell leukemia/lymphoma-2 proteins includes 2 types of antiapoptotic members, such as Bcl-2 Study Design and Bcl-xL, as well as proapoptotic members, such as the The rats were randomly assigned to 4 groups. The first multi-Bcl-2 homology- (BH-) and domain proteins Bax was a control group with a normal diet (ND). The second and Bak, and is the mediating factor of the mitochondria- group had a high-cholesterol diet (HD); 2% cholesterol dependent apoptosis pathway (16). The Bcl-2 proteins was given through regular food and water for 2 months. act as major regulators of basic and non-basic signaling Cholesterol with > 99.9% purity was purchased from pathways of apoptosis. These proteins can be used as Sigma Chemical Co. (St. Louis, MO, USA). The third therapeutic targets in the treatment of atherosclerosis group had a diet of combined high cholesterol and thymol (17). The mitochondrial pathway is triggered by proteins (HD+T); the animals received thymol with 2% cholesterol of the Bcl2 family or ions of Bak and Bax, whereas the (t0501; Sigma, St. Louis, MO, USA) at a dose of 24 mg/kg extrinsic pathway is triggered by the tumor necrosis factor for 2 months. The fourth group was the thymol group (T). (TNF) family or the activation of caspase 8, followed by the activation of caspase 3 (18-20). Sampling Thymol and carvacrol are 2 important natural Twenty-four hours after the last intervention and after 12 terpenoids that have antibacterial, antioxidant, and hours of fasting, the mice were deeply anesthetized by an anti-inflammatory
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