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Saffron (Crocus Sativus L.) Increases Glucose Uptake and Insulin Sensitivity in Muscle Cells Via Multipathway Mechanisms

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Saffron (Crocus Sativus L.) Increases Glucose Uptake and Insulin Sensitivity in Muscle Cells Via Multipathway Mechanisms Food Chemistry 135 (2012) 2350–2358 Contents lists available at SciVerse ScienceDirect Food Chemistry journal homepage: www.elsevier.com/locate/foodchem Saffron (Crocus sativus L.) increases glucose uptake and insulin sensitivity in muscle cells via multipathway mechanisms Changkeun Kang a, Hyunkyoung Lee a, Eun-Sun Jung a, Ramin Seyedian a,1, MiNa Jo a, Jehein Kim a, ⇑ Jong-Shu Kim a, Euikyung Kim a,b, a College of Veterinary Medicine, Gyeongsang National University, Jinju 660-701, South Korea b Research Institute of Life Science, Gyeongsang National University, South Korea article info abstract Article history: Saffron (Crocus sativus Linn.) has been an important subject of research in the past two decades because of Received 16 March 2012 its various biological properties, including anti-cancer, anti-inflammatory, and anti-atherosclerotic activ- Received in revised form 13 May 2012 ities. On the other hand, the molecular bases of its actions have been scarcely understood. Here, we elu- Accepted 25 June 2012 cidated the mechanism of the hypoglycemic actions of saffron through investigating its signaling Available online 3 July 2012 pathways associated with glucose metabolism in C2C12 skeletal muscle cells. Saffron strongly enhanced glucose uptake and the phosphorylation of AMPK (AMP-activated protein kinase)/ACC (acetyl-CoA car- Keywords: boxylase) and MAPKs (mitogen-activated protein kinases), but not PI 3-kinase (Phosphatidylinositol 3- Saffron kinase)/Akt. Interestingly, the co-treatment of saffron and insulin further improved the insulin sensitivity Glucose uptake Skeletal muscle cells via both insulin-independent (AMPK/ACC and MAPKs) and insulin-dependent (PI 3-kinase/Akt and AMPK mTOR) pathways. It also suggested that there is a crosstalk between the two signaling pathways of glu- Insulin sensitivity cose metabolism in skeletal muscle cells. These results could be confirmed from the findings of GLUT4 translocation. Taken together, AMPK plays a major role in the effects of saffron on glucose uptake and insulin sensitivity in skeletal muscle cells. Our study provides important insights for the possible mech- anism of action of saffron and its potential as a therapeutic agent in diabetic patients. Ó 2012 Elsevier Ltd. All rights reserved. 1. Introduction spices around the world for flavoring and coloring food (Sampathu, Shivashankar, Lewis, & Wood, 1984). It has also been applied in tra- Natural compounds with insulin-like activity (insulin mimetics) ditional medicine in the treatment of cramps, asthma and bron- have been proposed as potential therapeutic agents in the preven- chospasms, menstruation disorders, liver disease and pain tion and/or treatment of diabetes (Lee et al., 2006; Pinent et al., (Schmidt, Betti, & Hensel, 2007). Among the estimated more than 2008). They would act by promoting glucose transport and glucose 150 volatile and several nonvolatile compounds of saffron, major metabolism (Alberti, Zimmet, & Shaw, 2006). As the incidence and biologically active compounds are crocin, picocrocin, crocetin, car- prevalence of diabetes increase worldwide, there is a considerable otene and safranal (Rios, Recio, Giner, & Manez, 1996). Good qual- demand for therapeutic reagents which have a high efficacy and ity saffron contains about 30% crocin, 5–15% picocrocin, and low side effect profile. Therefore, screening for novel insulin usually up to 2.5% volatile compounds including safranal (Schmidt mimetics from various natural sources, such as plants and herbs, et al., 2007). The major constituents of saffron have attracted a are still attractive and some of them might be safely used on dia- considerable amount of interest during the past two decades and betes without causing serious side effects. shown both in vitro and in vivo to possess antioxidant, anti-cancer, Saffron, the dry stigmas of the plant Crocus sativus Linn., belong anti-inflammatory, anti-atherosclerosis and memory-improving to the Iridaceae family has been used as an important dietary properties (Abdullaev & Espinosa-Aguirre, 2004; Abe & Saito, ingredient in various parts of the world since ancient times. Fur- 2000; He et al., 2005; Hosseinzadeh & Younesi, 2002). Recently, thermore, saffron is one of the highest priced and the most used accumulating evidence has suggested the possibility of saffron being used as a candidate drug for diabetes. The hypoglycemic ef- fects of saffron were reported in a study involving diabetic rats ⇑ Corresponding author at: Department of Pharmacology and Toxicology, College (Mohajeri, Mousavi, & Doustar, 2009), but the molecular mecha- of Veterinary Medicine, Gyeongsang National University, 900 Gajwa-dong, Jinju nisms underlying this effect remain obscure. 660-701, South Korea. Tel.: +82 55 772 2355; fax: +82 55 772 2349. The glucose transport in skeletal muscle is regulated by two dis- E-mail address: [email protected] (E. Kim). 1 Department of Pharmacology and Toxicology, Bushehr University of Medical tinct pathways including phosphatidylinositol-3 kinase (PI 3-ki- Sciences, Bushehr, Iran. nase) and 50-AMP-activated protein kinase (AMPK) (Fig. 1). The PI 0308-8146/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.foodchem.2012.06.092 C. Kang et al. / Food Chemistry 135 (2012) 2350–2358 2351 Fig. 1. Schematic diagram of signaling pathways for the glucose metabolism of skeletal muscle cells and their pharmacological regulators. 3-kinase pathway includes activation of Akt leading to activation of ma–Aldrich Inc. (St. Louis, MO, USA). Antibodies for Phospho-Acet- glycogen synthesis and the other enzymes/proteins necessary for yl-CoA Carboxylase (Ser79), Phospho-AMPKa (Thr172), Phospho-Akt the acute metabolic effects of insulin, which promotes GLUT4 (Ser473), Phospho-Erk (Thr202), Phospho-p38 (Thr180), Phospho- translocation from an intracellular pool to plasma membrane SAPK/JNK (Thr183), AMPK, Akt and GLUT4 were obtained from Cell (Smith & Muscat, 2005). On the other hand, AMPK is a phylogenet- Signaling Technology (Beverly, MA). Compound C and LY294002 ically conserved intracellular energy sensor that plays a central were purchased from Calbiochem (Merck, Darmstadt, Germany). role in the regulation of glucose and lipid metabolism (Carling, 2-Deoxy-D [3H] glucose was obtained from Perkin-Elmer Life Sci- 2004). Activation of AMPK leads to the phosphorylation and regu- ences (Boston, MA, USA). All other reagents used were of the purest lation of a number of downstream targets that are involved in di- grade available. verse pathways, including acetyl-CoA carboxylase (ACC) in the body (Fryer & Carling, 2005). Both distinct pathways also increase the phosphorylation and activity of mitogen-activated protein ki- 2.2. Plant material and extraction nase (MAPK) family components, which participates in the full activation of insulin-stimulated glucose uptake via GLUT4 translo- The saffron was obtained from Saharkhiz Co. (Mashhad, Iran). cation (Konrad et al., 2001). After grinding the saffron stigmas, 2 g of dried stigma was ex- In the present study, we showed that saffron activates AMPK/ tracted with 100 ml of methanol (80%) for 2 h in an ultrasonic bath, ACC and stimulate glucose uptake in C2C12 skeletal muscle cells. and then shaken (110 rpm) for 12 h at room temperature. After the In addition, saffron enhanced insulin sensitivity in glucose metab- extraction, the methanol was evaporated using rotary vacuum olism via activation of AMPK/ACC, MAPKs, PI 3-kinase/Akt and evaporator (Tokyo Rikakikai Co., Ltd., Tokyo, Japan). The final aque- GLUT4 translocation to the plasma membrane. We further showed ous part was lyophilized and kept at À20 °C until use. The yield of that mTOR and its downstream pathway are also involved in this extraction was around 47% (w/w). process. Taken together, our results provide new insights into pos- sible mechanism of action by which saffron may contribute to the pharmacological intervention of diabetes. 2.3. Cell culture C2C12 (mouse myoblasts cell line) were maintained in DMEM 2. Materials and methods supplemented with 10% heat inactivated FBS and 1% antibiotics (100 U/ml penicillin and 100 lg/ml streptomycin), at 37 °Cina 2.1. Chemicals and reagents humidified atmosphere with 5% CO2. For differentiation into myo- tubes, cells were reseeded in 6-well plates (for immunoblotting), Dulbecco’s Modified Eagle’s Medium (DMEM), foetal bovine ser- and 12-well plates (for glucose uptake) at a density of um (FBS), bovine serum albumin (BSA), penicillin, streptomycin, 2 Â 104 cells/ml. After 48 h (over 80% confluence), the medium trypsin were obtained from Gibco-BRL (Grand Island, NY, USA). Di- was switched to DMEM with 2% (v/v) FBS and was replaced after methyl sulphoxide (DMSO), 3-(4,5-dimethylthiazol-2-yl)-2,5- 2, 4 and 6 days of culture. Experiments were initiated on day 7 diphenyltetrazolium bromide (MTT) were purchased from Sig- when myotube differentiation was complete. 2352 C. Kang et al. / Food Chemistry 135 (2012) 2350–2358 2.4. Cytotoxicity assay concentrations in cell lysates were measured using a Bio-Rad pro- tein assay reagent (Bio-Rad, CA, USA). Proteins in cultured cell ly- Cytotoxicity experiments were conducted to determine the sates (30–40 lg) were separated on 12% SDS–polyacrylamide gel, maximal nontoxic dose of saffron. Cell morphology was assessed transferred to PVDF membranes (Bio-Rad, CA, USA), and subse- by using phase-contrast microscopy, and viability was evaluated quently subjected to immunoblot analysis using specific primary by means of MTT assay (Mosmann,
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