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The effects of Korean mistletoe extract on endurance during exercise in mice The effects of Korean mistletoe extract on endurance during exercise in mice
Lee, Shin-Hae; Kim, In-Bo; Kim, Jong-Bae; Park, Dong-Ho; Min, Kyung-Jin
2014-01-02 00:00:00
Animal Cells and Systems, 2014 Vol. 18, No. 1, 34–40, http://dx.doi.org/10.1080/19768354.2014.881917 a† b† b c* a* Shin-Hae Lee , In-Bo Kim , Jong-Bae Kim , Dong-Ho Park and Kyung-Jin Min a b Department of Biological Sciences, Inha University, Incheon 402-751, Korea; School of Life Science, Handong Global University, Pohang 791-708, Korea; Major in Kinesiology, Division of Arts and Sports, Inha University, Incheon 402-751, Korea (Received 31 October 2013; received in revised form 31 December 2013; accepted 7 January 2014) Many investigators have screened drugs and foods for the enhancement of endurance capacity and antifatigue. Mistletoe, a semiparasitic plant on various deciduous trees, has many known biological activities, including anticancer, anti-diabetes, antioxidant, and anti-cardiovascular disease effects. In a previous study, Korean mistletoe extract (KME) was reported to increase endurance capacity in mice. However, whether the administration of KME further enhances exercise performance, when combined with exercise training, was not investigated. In this study, we demonstrate that the administration of KME decreases the level of plasma lactate dehydrogenase, parameter of tissue damage and muscle fatigue when combined with exercise training. Exercise training increases the muscular glycogen and plasma free fatty acid (FFA) level, and KME administration in sedentary mouse group increases the plasma FFA level, indicating that KME administration alters the energy resources in muscle. In addition, KME administration enhances the exercise performance in sedentary mouse group, but did not further enhance exercise performance when combined with exercise training, suggesting that KME could be an excellent mimetic of exercise. Keywords: exercise; endurance; mistltoe extract; energy utilization Introduction Mistletoe is a semiparasitic plant on various deciduous trees that has long been traditionally used, especially by The development of ergogenic supplements to improve Europeans, for preventing the progression of cancer. Mis- the physical performance of athletes has been actively tletoe has been demonstrated to have the lots of many conducted since the 1980s, and many investigators have biological activities, such as anticancer, anti-diabetes, and screened drugs and foods for their ability to enhance anti-cardiovascular disease effects. In addition, mistletoe endurance capacity. The ergogenic supplements that have extract was reported to have a high antioxidant activity, received the most attention in athletes are fish oils, such as even higher than vitamin C (Song et al. 2004). The omega-3 fatty acid, and nonsteroidal anti-inflammatory administration of Korean mistletoe (Viscum album color- drugs (NSAIDs). Omega-3 fatty acids have been reported atum) extract (KME) reportedly has benefits on blood to increase exercise performance via a decrease in inflam- lipid composition similar to exercise training, and mation (Mickleborough 2013) and reduce tissue damage decreases plasma ammonia levels, one of the causes of induced by exercise (Tartibian et al. 2011). NSAIDs are muscle fatigue (Kim & Kim 2009). In addition, KME has usually administrated to alleviate muscle soreness after recently been demonstrated to increase endurance capacity exercise (Schoenfeld 2012). In addition, L-carnitine was of mouse via the improvement of mitochondrial biogen- reported to decrease the muscle fatigue induced by acute esis (Jung et al. 2012). In that report, KME administration exercise (Pandareesh & Anand 2013), and the administra- increased the running, or swimming, time and distance tion of non-essential amino acid citrulline showed an until exhaustion, and decreased plasma lactate levels. increased swimming time until exhaustion and reduced However, whether the administration of KME further muscle fatigue (Takeda et al. 2011). Resveratrol, the active enhances exercise performance when combined with compound of red grapes, has been shown to improve exercise training was not investigated. Since major con- exercise performance and oxygen consumption, and sumers of ergogenic supplements for the enhancement of these effects were mediated by the activation of mitochon- exercise performance are athletes and those who perform a drial biogenesis (Dolinsky et al. 2012). However, inves- great deal of exercise, it is important to investigate tigations regarding the effects of phytoextracts, such as whether the effects of KME on exercise performance are Acanthopanax, Panax ginseng, and Cordyceps militaris, further improved when combined with exercise training. traditionally administrated by many athletes for exercise In this study, the effect of KME administration on performance are relatively fewer and their results are exercise endurance, muscle fatigue, and alterations in the controversial (Martinez & Staba 1984; Jung et al. 2004, 2007; Huang et al. 2011). fuel utilization of muscle were investigated. In addition, *Corresponding authors. Emails: dparkosu@inha.ac.kr; minkj@inha.ac.kr Both Shin-Hae Lee and In-Bo Kim contributed equally to this work. © 2014 Korean Society for Integrative Biology NEUROBIOLOGY & PHYSIOLOGY Animal Cells and Systems 35 whether KME administration further enhances exercise prepared by centrifugation at 2500 g at 4°C for 10 min performance, when combined with exercise training, was and then stored at –80°C. The levels of plasma free fatty examined. acids (FFAs) were analyzed with a commercial kit, the TM EnzyChrom Free Acid Assay Kit (BioAssay system). The levels of plasma lactate dehydrogenase (LDH), Materials and methods creatine kinase (CK), and cholesterol were analyzed with Extraction of Korean mistletoe the Auto Chemistry Equalizer (Mindray, BS-390). All experiments were carried out with materials derived from Korean mistletoe (Viscum album coloratum) plants Endurance test grown on a local oak tree (Quercus variabilis Blume). The After 2 weeks of KME administration and/or exercise leaves of the Korean mistletoe plants were homogenized training, mice starved for 2 hrs performed an endurance and boiled for 3 hrs in 10 volumes of distilled water. The test on a treadmill (Columbus Instruments) enclosed in a extract was centrifuged at 8000 rpm for 10 min, and the plexiglass chamber outfitted with a shock grid at the rear suspension filtered through 0.45-µm filter paper (What- of the belt to keep the animal running during the test. The man plc, UK). The filtrate was lyophilized and kept in a shock grid delivered a 0.2 mA shock, which was deep freezer at –80°C before use. uncomfortable but did not physically harm or injure the animals. The animals were habituated to the test condi- Animal care tions before experimentation. During the test procedure, Pathogen-free 12-week-old male impriting control region the mice ran on a treadmill with a 0° incline at a speed of (ICR) mice were purchased from Hyochang Science (www. 22 m/min to exhaustion. When the mice reached exhaus- dhbiolink.com). All animal experiments were approved tion defined by the inability to run for 10 sec (Hakimi through the Ethics Review Committee of Handong Global et al. 2007), the electric shock was discontinued and the University, Republic of Korea. The mice were given access time and distance to exhaustion was counted. to water and dried chow (KKW1Q0124; Cheil Feed Corp.) ad libitum until endurance tests were completed. Measurement of muscular glycogen content Immediately after blood collection, the quadriceps femoris Supplementation of KME muscles were quickly dissected out and kept at –80°C Thirty-two mice were divided into four groups (n = 8 per until analyzed for glycogen content. The glycogen content group): a non-administered sedentary control group (Con), was spectrophotometrically measured using the glucose a KME-administered sedentary group (KME), a non- oxidase method (Chun & Yin 1998). Briefly, after diges- administered running exercise training group (EX), and a tion of the muscle samples in 30% KOH at 100°C for 30 KME-administered and running exercise training group min, 1.5 mL of 95% alcohol was added to the vials. After (KME + EX). Two groups of mice (KME, KME + EX) centrifugation at 3000 rpm for 10 min, the supernatant were orally administered KME (500 mg/kg), and the other was discarded; the residue was then suspended in 0.5 mL two groups (Con, EX) were administered PBS for 2 weeks of distilled water, and 1 mL of 0.2% anthrone in H SO 2 4 before experiments. was added. The vials were placed in a boiling water bath for 30 min. The absorbance for the solution was determined using a FLUOstar OPTIMA microtiter plate Exercise protocol reader (BMG Labtech GmbH) at a 620-nm wavelength. Two groups of mice (EX, KME + EX) were acclimatized to the treadmill (Columbus Instruments) by running 7 days before main exercise training for 10 min at 8 m/min. Statistical analyses The running exercise training consisted of daily running Data were presented as the mean ± SEM, and statistical for 30–40 min (10–22 m/min, 5 days a week) for 2 weeks. analyses data were carried out using one-way analysis of variance. Analysis of blood biochemical parameters After 2 weeks of KME supplementation and/or exercise Results training, the mice performed an endurance test on a KME decreases muscle fatigue in exercise-trained mice treadmill until exhaustion. The mice were then sacrificed after 3 days to settle down. After euthanasia using CO After high-intensity exercise, muscle fatigue accumulates; gas, whole blood samples were collected from mice in a thus, the ability to decrease muscle fatigue is important vacutainer tube and then prepared with sodium fluoride for the enhancement of exercise performance. During and potassium oxalate by heart puncture. Plasma was extensive physical exercise, excessive free radicals are 36 S.-H. Lee et al. p = 0.71 2000 6 p = 0.3 p < 0.05 p < 0.05 p = 0.22 p = 0.36 p = 0.42 1000 3 p = 0.94 Con KME EX KME + EX Con KME EX KME + EX Figure 1. Effect of KME on muscle fatigue in exercise-trained mice. The levels of plasma lactate dehydrogenase (A, LDH) and creatine kinase (B, CK) in mice, given either vehicle or KME (500 mg/kg/day) for 2 weeks, and trained (or not) on a treadmill for 2 weeks were examined. KME administration decreased the levels of plasma LDH in the exercise-trained mice but did not affect the levels of CK. generated, which lead to tissue damage and the leakage of physical fatigue caused by high-intensity exercise when several cytosolic enzymes, such as LDH and CK, into sera combined with exercise training. Unexpectedly, plasma (Van Hall 2000; Brancaccio et al. 2007). Therefore, those levels of CK were not significantly altered through enzymes can be good parameters for tissue damage and exercise training or the combination of exercise training muscle fatigue. To investigate whether the supplementa- with KME administration (Figure 1B). tion of KME decreases muscle fatigue, fatigue-related KME decreases total cholesterol and high-density biochemical parameters were evaluated. Mice were lipoprotein cholesterol (HDL-C) levels in exercise-trained divided into four experimental groups (n = 8 each one). mice. Two groups of mice (EX, KME + EX) were trained on a Previous reports showed that KME administration treadmill for 2 weeks, and two groups of mice (KME, enhances blood lipid profiles. Methanol or ethanol extracts KME + EX) were fed KME 500 mg/kg/day. After 2 weeks of mistletoe were reported to decrease total plasma of KME administration and/or exercise training, mice in cholesterol levels (Avci et al. 2006; Ferrero et al. 2007; the four groups performed the endurance test using a Bachhav et al. 2012) and increase HDL-C levels (Avci treadmill until exhaustion, and then the blood levels of et al. 2006; Ben et al. 2006; Adaramoye et al. 2012)in LDH and CK were analyzed. In the sedentary condition, mice or rats. However, the effect of an aqueous extract of KME supplementation did not affect the level of LDH Korean mistletoe on the plasma levels of cholesterol and (Figure 1A, p = 0.42) and CK (Figure 1A, p = 0.94) HDL-C was controversial (Kim 2006; Kim & Kim 2009). compared to the non-administered Con. However, the To investigate the effect of KME administration on levels of LDH significantly increased almost 2 times cholesterol levels, the plasma level of total cholesterol through exercise training compared with sedentary mice and HDL-C of the four experimental groups of mice (Figure 1A, p < 0.05). This enhancement of LDH levels described above were analyzed after the treadmill endur- by exercise training was reduced when exercise training ance test until exhaustion. In sedentary conditions, the was combined with KME administration (Figure 1A, 43% administration of KME did not affect the levels of total compared with exercise training only, p < 0.05). This cholesterol and HDL-C (Figure 2, cholesterol p = 0.41; result suggests that KME administration reduced the HDL-C p = 0.15) compared with non-administered control A B 140 160 p < 0.05 p < 0.0001 130 140 p < 0.001 p < 0.05 p < 0.0001 p < 0.05 120 120 p = 0.41 110 100 100 80 p = 0.15 90 60 80 40 70 20 Con KME EX KME + EX Con KME EX KME + EX Figure 2. Effect of KME on cholesterol levels in exercise-trained mice. The levels of plasma total cholesterol (A) and high-density lipoprotein (HDL) cholesterol (B) of mice given either vehicle or KME (500 mg/kg/day) for 2 weeks, and trained (or not) on a treadmill for 2 weeks were examined. KME administration reduced the levels of total cholesterol and HDL-C during exercise training. Cholesterol (mg/dL) LDH (U/L) HDL-C (mg/dL) CK (g/L) Animal Cells and Systems 37 AB p < 0.0042 6 p < 0.0042 p = 0.241 p = 0.241 p < 0.005 250 5 p < 0.0017 p < 0.015 p < 0.015 200 4 150 3 50 1 0 0 Con KME EX KME + EX Con KME EX KME + EX Figure 3. Combined effect of KME administration and exercise training on endurance capacity. KME administration or exercise training increased the running time (A) and distance (B) to exhaustion. However, the combination of KME administration and exercise training for 2 weeks did not show a synergic effect on the endurance capacity. Gray bars: basal capacity of exercise performance before treatments. Black bars: endurance capacity after treatments. mice. Exercise training increased the levels of total choles- previous report, muscular glycogen levels decreased terol and HDL-C (Figure 2, cholesterol p < 0.001; HDL-C through the administration of 1000 mg/kg/day KME for p < 0.0001). The administration of KME together with 1 week but remained unchanged through the administra- exercise training significantly decreased the levels of total tion of 400 mg/kg/day KME (Jung et al. 2012). Similarly, cholesterol and HDL-C (Figure 2, cholesterol p < 0.05; HDL-C p < 0.05) compared with exercise-trained mice. p = 0.26 p < 0.05 p = 0.29 Effect of KME administration during exercise training on endurance The endurance performance of mice was examined using a p = 0.52 treadmill until exhaustion. Similar to a previous report (Jung et al. 2012), the administration of KME increased the running time and distance to exhaustion almost 1.3 times compared to the vehicle-treated sedentary group (Figure 3, p < 0.015). In addition, 2 weeks of exercise training also increased exercise endurance almost 1.5 times compared to the sedentary group (Figure 3, p < 0.005). However, the Con KME EX KME + EX combination of KME administration and exercise training p < 0.05 did not further increase exercise endurance compared to B 1.4 exercise training alone (Figure 3, p = 0.241). p < 0.0001 p = 0.076 1.3 p < 0.001 Effect of KME on the utilization of energy resources in 1.2 exercise-trained mice 1.1 Glucose and fatty acids are the main fuel sources for skeletal muscle during exercise. However, during high- 1.0 intensity exercise, the main energy resources are muscular glycogen; thus, glycogen levels in muscle decrease during 0.9 high-intensity exercise. It is important to save muscular glycogen, through changing energy resources to fatty 0.8 Con KME EX KME + EX acids, for the enhancement of exercise performance (Hawley 2002). To clarify whether KME administration Figure 4. Effect of KME on the utilization of energy resources can modify the glycogen utilization rate, the levels of during exercise training. After mice were given either vehicle or KME (500 mg/kg/day) for 2 weeks and trained (or not) on a muscular glycogen and plasma FFAs were assessed after treadmill for 2 weeks, the levels of muscular glycogen (A) and high-intensity exercise. Two weeks of exercise training plasma FFAs (B) were analyzed. KME administration or exercise significantly increased the levels of muscular glycogen training increased the levels of muscular glycogen and plasma (Figure 4A, 23% increase, p < 0.05) and plasma FFA FFAs, but the combination of KME administration and exercise (Figure 4B, 19% increase, p < 0.0001) after the treadmill training did not show a synergic effect on changes in energy resource utilization. endurance test compared with the sedentary Con. In a Time (min) Distance (Km) FFA (µg/ml) Glycogen (µg/ml) 38 S.-H. Lee et al. in our sedentary condition, 500 mg/kg/day KME admin- healthy humans (Messonnier et al. 2005). However, under istration for 2 weeks did not affect the muscular glycogen our experimental condition, the plasma LDH levels of level (Figure 4A, p = 0.52). However, the administration exercise-trained mice were greater than those of sedentary of KME increased the plasma level of FFA (Figure 4B, control mice after high-intensity exercise (Figure 2). 14% increase, p < 0.001), indicating that KME has the Although further investigations are required, higher levels ability to alter the utilization of muscular energy resources of LDH in our study may be caused by difference in from glycogen to fatty acids. Consistent with the results duration or strength of exercise training or collection time from the exercise endurance test, the combination of KME of blood sample. administration and exercise training did not show additive Many studies have demonstrated the beneficial effects beneficial effects on energy source utilization changes of mistletoe extracts on blood lipid profiles and cardio- from glycogen to fatty acids compared to exercise training vascular risk. However, under our sedentary condition, the alone (Figure 4, p = 0.29). plasma levels of total cholesterol and HDL-C were unaffected by KME administration (Figure 2). Mistletoe contains numerous bioactive compounds, including lec- Discussion tins, alkaloids, viscotoxins, and polysaccharides (Khwaja In this study, the beneficial effects of KME, combined et al. 1980, 1986; Holtskog et al. 1988), and their with exercise training, on exercise performance were biological effects are known to be changed according to examined. We found that KME administration had bene- their preparation, host trees, and harvest times (Hulsen & ficial effects on the accumulation of muscle fatigue and Mechelke 1982; Park et al. 1999). Previous reports blood cholesterol levels when combined with exercise showed the beneficial effects of mistletoe on blood training. In addition, KME administration increased exer- cholesterol levels using methanol or ethanol mistletoe cise endurance in sedentary mice but did not affect extracts (Avci et al. 2006; Ferrero et al. 2007; Bachhav exercise endurance combined with exercise training. et al. 2012); however, an aqueous extract of mistletoe was A recent report demonstrated that the administration of used in this study. Thus, the different effects of mistletoe 400 or 1000 mg/kg/day KME improves the exercise extracts on plasma cholesterol levels between our study endurance of 12-week-old mice in the treadmill running and previous reports may be caused by different extract test and swimming test (Jung et al. 2012). The oral preparations which may lead to a different composition of administration of KME in that report decreased the levels bioactive compounds. of plasma glucose and lactate, increased oxygen con- The level of HDL-C was reported to increase by sumption rate, and increased the mRNA expression of exercise training (Kodama et al. 2007; Musa et al. 2009), genes related to mitochondrial biogenesis and function but the effect of exercise training on the level of total (such as PGC-1α and SIRT1) in rat myoblast cells. cholesterol is controversial (Durstine et al. 2001; Fahlman However, that report did not verify the effect of KME et al. 2002). In our experiments, both of the total administration combined with exercise training on exer- cholesterol and HDL-C levels were increased through cise performance, which is important from an athlete’s exercise training (Figure 2). The increase in total choles- point of view. terol may be caused by the excessive elevation of HDL-C We found that KME administration had a beneficial through exercise training. The administration of KME effect on the accumulation of muscle fatigue, as indicated slightly reduced the level of HDL-C when it was combined through its impact on the plasma levels of LDH (Figure 1). with exercise training compared to that of exercise-trained In the sedentary condition, KME administration tended to non-administrated mice; however, the level of plasma decrease plasma LDH levels almost 20% compared to the HDL-C in the KME-administrated/exercise-trained mice non-administered Con; however, this decrease was not was definitely increased compared to non-administrated/ statistically significant (p = 0.42). Under the exercise sedentary mice group. training condition, KME administration significantly Our results indicate that KME administration has decreased plasma LDH levels. Consistent with our data, beneficial effects on muscle fatigue accumulation and previous reports showed that mistletoe had an greater lipid profiles during exercise training. However, the antioxidant activity compared to vitamin C (Song et al. combination of KME administration with exercise training 2004) and decreased the plasma NH level in exercise- did not further increase the exercise endurance capacity trained mice (Kim & Kim 2009). Since reactive oxygen (Figure 3). A recent study showed that the agonist of species and ammonia are main causes of muscle fatigue, AMPK, 5-aminoimidazole-4-carboxamide ribonucleoside our data and these previous reports indicate the beneficial (AICAR), improved exercise endurance and modified effect of KME on the accumulation of muscle fatigue. In gene expression profiles (including uncoupled protein 3 the previous reports, long-term exercise training (3–4 [UCP3]); similar to the benefits of exercise training weeks) was reported to decrease the plasma levels of without practical exercise training (Narkar et al. 2008). LDH in heart failure patients (Mammi et al. 2011) and Thus, they concluded that AICAR is a mimetic of Animal Cells and Systems 39 muscle strength and cardiac function induced by resveratrol exercise. Similar to AICAR, KME administration was during exercise training contribute to enhanced exercise sufficient in the enhancement of exercise endurance capa- performance in rats. J Physiol. 590:2783–2799. city without exercise training. In addition, we found that Durstine JL, Grandjean PW, Davis PG, Ferguson MA, Alderson KME treatment also increased the expression of UCP3 in NL, DuBose KD. 2001. Blood lipid and lipoprotein adapta- the rat myoblast cell line and one of the bioactive tions to exercise: a quantitative analysis. Sports Med (Auckland, NZ). 31:1033–1062. compounds of KME can activate AMPK in an in vitro Fahlman MM, Boardley D, Lambert CP, Flynn MG. 2002. system similarly to AICAR (data not shown). 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