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Exercise-Induced Changes in Amino Acid Levels in Skeletal Muscle and Plasma

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Exercise-Induced Changes in Amino Acid Levels in Skeletal Muscle and Plasma J Phys Fitness Sports Med, 2(3): 301-310 (2013) DOI: 10.7600/jpfsm.2.301 JPFSM: Review Article Exercise-induced changes in amino acid levels in skeletal muscle and plasma Keisuke Ishikura1†, Song-Gyu Ra2,3† and Hajime Ohmori4* 1 Sports Research and Development Core, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8574, Japan 2 Graduate School of Comprehensive Human Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8574, Japan 3 Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan 4 Faculty of Health and Sport Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8574, Japan Received: June 25, 2013 / Accepted: July 25, 2013 Abstract During exercise, amino acid oxidation and protein breakdown are enhanced while protein synthesis is suppressed, even though protein does not constitute a quantitatively impor- tant energy source. In response to exercise-induced stimulation, various changes in free amino acids occur in skeletal muscle to meet physiological demands. Plasma amino acids are also under the influence of various types of stress, including exercise stress. For example, acute ex- ercise increases alanine and glutamine levels, but decreases glutamate levels in skeletal muscle. At the same time, it increases tryptophan and taurine levels, but decreases glutamine levels in plasma. Prolonged exercise decreases glutamine and glutamate levels, while increasing tyrosine and phenylalanine levels in skeletal muscle. Furthermore, when prolonged exercise-induced changes in amino acid levels are compared between trained and untrained individuals, gluta- mate and taurine levels in skeletal muscle and phenylalanine, leucine, isoleucine, and tyrosine levels in plasma are higher in trained individuals. This review provides an overview of changes in amino acid levels in skeletal muscle and plasma, with a focus on changes induced by exer- cise. Keywords : amino acids, skeletal muscle, plasma, exercise prolonged period of starvation. Exercise-induced drastic Introduction glycogen depletion has a similar effect as starvation. For Ingested protein is digested and eventually broken down example, the body utilizes amino acids of muscle protein to amino acids. Proteins in the body are composed of origin as a fuel source during exercise after depletion of about 20 types of amino acids, and skeletal muscle pro- muscle glycogen, as demonstrated by the cycle ergometer tein makes up more than 60% of whole-body protein1). experiment4). Although amino acid utilization in exercise- Individual tissues release amino acids generated via deg- induced increases in metabolic processes, such as hepatic radation of old tissue proteins, while the small intestine gluconeogenesis and the tricarboxylic acid cycle (TCA), absorbs amino acids of dietary origin, which are subse- is a secondary event, it is well known that hepatic gluco- quently assimilated by the body. This mixture of amino neogenesis increases depending on exercise intensity and acids originating from both degradation of tissue protein duration5,6). Furthermore, the glucose–alanine cycle is im- and dietary protein is called the amino acid pool (Fig. 1). portant for regenerating glucose through gluconeogenesis Amino acids of this pool exist in plasma, lymphatic fluid, in the liver and returning it to muscle through circulation7) interstitial fluid, and intracellular fluid, and their levels are (Fig. 2). kept constant. In addition to being used for protein synthe- In addition to various organs, blood plasma also serves sis, a considerable proportion of amino acids in the pool is as a temporary reservoir of amino acids. Amino acid used as an energy source after degradation and oxidation, levels in plasma, as well as those in organs, change in re- and their degradation products are eventually excreted. sponse to various types of stress. Stress is one of the fac- During exercise, amino acid catabolism is elevated2), al- tors associated with the onset of various diseases such as though protein is generally not a main energy fuel3). Pro- diabetes and liver disease, and profiles of plasma amino tein, including that of muscle tissue origin, serves as an acid levels are known to differ between patients and important fuel source in muscle energy metabolism only healthy individuals8-10). Exercise can be considered a type when the normal energy supply is limited, such as after a of stress, and indeed, differences in regular exercise and daily activities result in differences in plasma amino acid 11,12) *Correspondence: [email protected] levels . †Authors contributed equally to this paper and are listed Exercise enhances amino acid oxidation and protein in alphabetical order. breakdown. During prolonged exercise, amino acids are 302 JPFSM: Ishikura K, et al. Tissue Protein Energy production Dietary Amino Acid Triglyceride and protein Pool Carbohydrate Urine (Urea, Uric acid and Creatinine) Fig. 1 Amino acid pool. Cells throughout the body constantly synthesize and breakdown protein. Individual tissues release amino acids generated via degradation of tissue proteins, and the small intestine absorbs amino acids of dietary origin. Subsequently, amino acids are released into circulation. This mixture of amino acids of different origins is called the amino acid pool, and exists in the plasma, lymphatic fluid, interstitial fluid, and intracellular fluid. In addition to being used for protein synthesis, a consider- able proportion of amino acids in the pool is used as an energy source after degradation and oxidation, and degradation products are eventually excreted. delivered to the liver through the bloodstream to satisfy 23 free amino acids in slow-twitch muscles is twice as the increased local demands for amino acids. This re- high as that in fast-twitch muscles in rat skeletal muscle17). view outlines how amino acid levels in skeletal muscle However, intracellular amino acid levels are known to and plasma change in response to exercise- and disease- differ between fast-twitch muscle fibers and slow-twitch related stress. muscle fibers. For example, the slow fiber-rich soleus has levels of an essential amino acid (histidine), several non- essential amino acids (glutamine, glutamate, aspartate, Amino acid pool in skeletal muscle and serine), and other amino acids (taurine, citrulline, Amino acids derived by the breakdown of dietary and phosphoserine, and ornithine) that are 57 - 87% higher tissue proteins are stored in the amino acid pool before than those in the fast fiber-rich plantaris and gastrocne- being utilized for protein synthesis or catabolized. Post- mius. On the other hand, fast-twitch fiber-rich muscles prandial increases in plasma amino acid levels stimulate show higher concentrations of two essential amino acids protein synthesis, while, during exercise, protein syn- (glycine and alanine) than slow-twitch fiber-rich muscles. thesis in skeletal muscle is decreased13-15) and protein Profiles of free amino acid levels in humans appear to degradation is elevated15). In addition, endurance exercise differ from the above levels in rats. Glutamate, aspartate, increases amino acid oxidation16). In general, there are and arginine levels are reportedly 10% higher in type II three ways of increasing free amino acid levels in skeletal than in type I fibers in endurance cyclists20). Considering muscle: (a) degradation of muscle protein; (b) conver- that muscle amino acids levels are under the influence of sion from other amino acids and intermediates; and (c) physical activity, the above differences between humans uptake from extracellular fluid. Conversely, there are also and rats may be attributed to differences in muscle train- three ways to decrease free amino acid levels in skeletal ing status20). muscle: (a) release into the extracellular fluid; (b) resyn- thesize into proteins; and (c) muscle catabolism11). Here During and after exercise we provide an overview of the free amino acid levels in 1. Short-term exercise in rats skeletal muscle in resting condition, changes in levels Glutamate levels in rats decreased in response to 5-min induced by exercise, and the effect of training in both rats electrical stimulation, while alanine and pyruvate levels and humans. increased in contracting gastrocnemius muscles; simi- larly, glutamate levels decreased, but alanine and aspar- In resting condition tate levels increased in contracting soleus muscles22). 1. Amino acid levels in skeletal muscle Decreases in glutamate levels and increases in alanine Of the free amino acids in skeletal muscle, glutamate levels, observed in both types of muscles, may be due and taurine are abundant in rodents17) and humans18-20). to the production of alanine via the glutamate-pyruvate transaminase (GPT)-catalyzed reaction, wherein an amino 2. Muscle fiber type differences group is transferred from glutamate to pyruvate produced The rates of protein synthesis and degradation are gen- by glycolysis to form alanine. The GPT-catalyzed reaction erally higher in slow-twitch muscles than in fast-twitch also produces α- ketoglutarate from glutamate, which is muscles in rats21). Furthermore, the total concentration of an important intermediate in the TCA cycle23). Decreases JPFSM: Amino acids in skeletal muscle and plasma 303 ・ in glutamate levels and increases in aspartate levels, ob- during exercise with a load of 30% VO2max and remained served in the soleus muscle, suggest production of aspar- constant regardless of increasing workloads. Such
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