Effects of voluntary wheel running and amino acid supplementation on skeletal muscle of mice

The aims of the present study were as follows: (1) to examine the adaptational changes to chronic endurance voluntary exercise and (2) to investigate the effects of amino acid supplementation on the adaptational changes induced by endurance training in hindlimb (gastrocnemius, tibialis, soleus) and respiratory (diaphragm) muscles of mice. Male C57Bl6 mice were divided in four groups: control sedentary, sedentary supplemented with amino acid mixture (BigOne, 1.5 mg g day−1 in drinking water for 8 weeks), running (free access to running wheels for 8 weeks), and running supplemented with amino acid mixture. Myosin heavy chain (MHC) isoform distribution was determined in all muscles considered. Fiber cross-sectional area (CSA) was measured in the soleus muscle. In all muscles except the tibialis, endurance training was associated with an overall shift towards the expression of slower MHC isoforms. Amino acid supplementation produced a shift towards the expression of faster MHC isoforms in the soleus and diaphragm muscles, and partially antagonized the effects of training. Immunohistochemical analysis of CSA of individual muscle fibers from the soleus muscle suggests that voluntary running produced a decrease in the size of type 1 fibers, and amino acid supplementation during training resulted in an increase in size in both type 1 and type 2A fibers. Collectively, these results suggest that the endurance adaptations induced by voluntary running depend on the muscle type, and that amino acid supplementation is able to modulate both fiber size and MHC isoform composition of skeletal muscles in sedentary and exercised mice.

[1]  R. Wolfe,et al.  Postexercise net protein synthesis in human muscle from orally administered amino acids. , 1999, American journal of physiology. Endocrinology and metabolism.

[2]  O. Pansarasa,et al.  "Oxidative stress": effects of mild endurance training and testosterone treatment on rat gastrocnemius muscle , 2002, European Journal of Applied Physiology.

[3]  D. Matthys,et al.  Effect of branched-chain amino acids (BCAA), glucose, and glucose plus BCAA on endurance performance in rats. , 1999, Medicine and science in sports and exercise.

[4]  C. Scrimgeour,et al.  Increase in anterior tibialis muscle protein synthesis in healthy man during mixed amino acid infusion: studies of incorporation of [1-13C]leucine. , 1989, Clinical science.

[5]  G. Biolo,et al.  An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. , 1997, The American journal of physiology.

[6]  T. Garland,et al.  Effects of voluntary activity and genetic selection on muscle metabolic capacities in house mice Mus domesticus. , 2000, Journal of applied physiology.

[7]  Ø. Ellingsen,et al.  Intensity-controlled treadmill running in mice: cardiac and skeletal muscle hypertrophy. , 2002, Journal of applied physiology.

[8]  K. Nair,et al.  Leucine as a regulator of whole body and skeletal muscle protein metabolism in humans. , 1992, The American journal of physiology.

[9]  D. Stephenson,et al.  Fiber type populations and Ca2+-activation properties of single fibers in soleus muscles from SHR and WKY rats. , 1999, American journal of physiology. Cell physiology.

[10]  O. Bonne,et al.  Behavioral and neurochemical alterations caused by diet restriction - the effect of tyrosine administration in mice , 1996, Brain Research.

[11]  B. Harrison,et al.  Skeletal muscle adaptations in response to voluntary wheel running in myosin heavy chain null mice. , 2002, Journal of applied physiology.

[12]  C. Reggiani,et al.  Orthologous myosin isoforms and scaling of shortening velocity with body size in mouse, rat, rabbit and human muscles , 2003, The Journal of physiology.

[13]  M. Bonifazi,et al.  Changes in the exercise-induced hormone response to branched chain amino acid administration , 2004, European Journal of Applied Physiology and Occupational Physiology.

[14]  W. Saris,et al.  Ingestion of branched‐chain amino acids and tryptophan during sustained exercise in man: failure to affect performance. , 1995, The Journal of physiology.

[15]  R. Fitts,et al.  Isometric force and maximal shortening velocity of single muscle fibers from elite master runners. , 1996, The American journal of physiology.

[16]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[17]  P. Flakoll,et al.  Postexercise protein intake enhances whole-body and leg protein accretion in humans. , 2002, Medicine and science in sports and exercise.

[18]  B. Saltin,et al.  BCAA intake affects protein metabolism in muscle after but not during exercise in humans. , 2001, American journal of physiology. Endocrinology and metabolism.

[19]  M. Kleiber Body size and metabolism , 1932 .

[20]  W. Cheadle,et al.  Time course adaptations in cardiac and skeletal muscle to different running programs. , 1977, Journal of applied physiology: respiratory, environmental and exercise physiology.

[21]  Nutritional supplementation and resistance exercise: what is the evidence for enhanced skeletal muscle hypertrophy? , 2000, Canadian journal of applied physiology = Revue canadienne de physiologie appliquee.

[22]  G. Margaritondo,et al.  Reactivity of Au with ultrathin Si layers: A photoemission study , 2001 .

[23]  R. Wolfe,et al.  An oral essential amino acid-carbohydrate supplement enhances muscle protein anabolism after resistance exercise. , 2000, Journal of applied physiology.

[24]  M. Kjaer,et al.  Timing of postexercise protein intake is important for muscle hypertrophy with resistance training in elderly humans , 2001, The Journal of physiology.

[25]  C. Reggiani,et al.  Human skeletal muscle fibres: molecular and functional diversity. , 2000, Progress in biophysics and molecular biology.

[26]  C. Reggiani,et al.  Force‐velocity relations and myosin heavy chain isoform compositions of skinned fibres from rat skeletal muscle. , 1991, The Journal of physiology.

[27]  P. Verger,et al.  Effects of administration of branched-chain amino acids vs. glucose during acute exercise in the rat , 1994, Physiology & Behavior.

[28]  A. Irintchev,et al.  Muscle injury, cross‐sectional area and fibre type distribution in mouse soleus after intermittent wheel‐running. , 1990, The Journal of physiology.

[29]  R R Roy,et al.  Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. , 1993, Journal of applied physiology.

[30]  B. Harrison,et al.  Cardiac and skeletal muscle adaptations to voluntary wheel running in the mouse. , 2001, Journal of applied physiology.

[31]  W. Haskell,et al.  Variations in running activity and enzymatic adaptations in voluntary running rats. , 1989, Journal of applied physiology.

[32]  S. Katsuta,et al.  The relationship of voluntary running to fibre type composition, fibre area and capillary supply in rat soleus and plantaris muscles , 2004, European Journal of Applied Physiology and Occupational Physiology.

[33]  C. Reggiani,et al.  Molecular diversity of myofibrillar proteins: gene regulation and functional significance. , 1996, Physiological reviews.

[34]  G. Biolo,et al.  Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. , 1995, The American journal of physiology.

[35]  P. Hassmén,et al.  Effect of branched-chain amino acid and carbohydrate supplementation on the exercise-induced change in plasma and muscle concentration of amino acids in human subjects. , 1995, Acta physiologica Scandinavica.

[36]  T. Sugiura,et al.  Myosin heavy chain isoform changes in rat diaphragm are induced by endurance training. , 1990, The Japanese journal of physiology.

[37]  J. Deijen,et al.  Effect of tyrosine on cognitive function and blood pressure under stress , 1994, Brain Research Bulletin.

[38]  K. A. Dougherty,et al.  Repeated development and regression of exercise-induced cardiac hypertrophy in rats. , 1983, Journal of applied physiology: respiratory, environmental and exercise physiology.

[39]  S. Powers,et al.  Exercise-induced alterations in skeletal muscle myosin heavy chain phenotype: dose-response relationship. , 1999, Journal of applied physiology.

[40]  M. Vukovich,et al.  Effects of a low-dose amino acid supplement on adaptations to cycling training in untrained individuals. , 1997, International journal of sport nutrition.

[41]  J. Holloszy Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. , 1967, The Journal of biological chemistry.

[42]  D. Perrett,et al.  Effect of sustained exercise on plasma amino acid concentrations and on 5-hydroxytryptamine metabolism in six different brain regions in the rat. , 1989, Acta physiologica Scandinavica.

[43]  S. Ward,et al.  Chronic fatigue syndrome: new evidence for a central fatigue disorder. , 2003, Clinical science.

[44]  F. Haddad,et al.  highlighted topics Plasticity in Skeletal, Cardiac, and Smooth Muscle Invited Review: Effects of different activity and inactivity paradigms on myosin heavy chain gene expression in striated muscle , 2000 .

[45]  R. Barnard,et al.  Adaptation of the rat myocardium to endurance training. , 1978, Journal of applied physiology: respiratory, environmental and exercise physiology.

[46]  T. Sugiura,et al.  Effects of endurance training on myosin heavy-chain isoforms and enzyme activity in the rat diaphragm , 1992, Pflügers Archiv.

[47]  C. Wientjes,et al.  Tyrosine improves cognitive performance and reduces blood pressure in cadets after one week of a combat training course , 1999, Brain Research Bulletin.

[48]  R. DeFronzo,et al.  Effect of insulin and plasma amino acid concentrations on leucine metabolism in man. Role of substrate availability on estimates of whole body protein synthesis. , 1987, The Journal of clinical investigation.

[49]  R. Fitts,et al.  Shortening velocity and ATPase activity of rat skeletal muscle fibers: effects of endurance exercise training. , 1994, The American journal of physiology.

[50]  T. Garland,et al.  Effects of genetic selection and voluntary activity on the medial gastrocnemius muscle in house mice. , 1999, Journal of applied physiology.

[51]  S. Powers,et al.  Myosin heavy chain composition in young and old rat skeletal muscle: effects of endurance exercise. , 1995, Journal of applied physiology.

[52]  E. Berry,et al.  Tyrosine improves appetite, cognition, and exercise tolerance in activity anorexia. , 2001, Medicine and science in sports and exercise.

[53]  G. Dudley,et al.  Influence of exercise intensity and duration on biochemical adaptations in skeletal muscle. , 1982, Journal of applied physiology: respiratory, environmental and exercise physiology.

[54]  D. Pette Training effects on the contractile apparatus. , 1998, Acta physiologica Scandinavica.

[55]  R. Wolfe,et al.  Exogenous amino acids stimulate net muscle protein synthesis in the elderly. , 1998, The Journal of clinical investigation.

[56]  F. Booth,et al.  Molecular and cellular adaptation of muscle in response to exercise: perspectives of various models. , 1991, Physiological reviews.

[57]  M. Rennie,et al.  Effects of flooding amino acids on incorporation of labeled amino acids into human muscle protein. , 1998, The American journal of physiology.

[58]  R. Fitts,et al.  The determinants of skeletal muscle force and power: their adaptability with changes in activity pattern. , 1991, Journal of biomechanics.

[59]  L. Baur,et al.  Relationships between muscle membrane lipids, fiber type, and enzyme activities in sedentary and exercised rats. , 1995, The American journal of physiology.

[60]  T. Garland,et al.  Effects of voluntary activity and genetic selection on aerobic capacity in house mice (Mus domesticus). , 1998, Journal of applied physiology.

[61]  P. Hassmén,et al.  Administration of branched-chain amino acids during sustained exercise — effects on performance and on plasma concentration of some amino acids , 2004, European Journal of Applied Physiology and Occupational Physiology.

[62]  Raul K. Suarez,et al.  Allometric cascade as a unifying principle of body mass effects on metabolism , 2002, Nature.

[63]  Jeffrey R Stout,et al.  Effects of exercise training and amino-acid supplementation on body composition and physical performance in untrained women. , 2000, Nutrition.

[64]  T. Garland,et al.  Exercise physiology of wild and random-bred laboratory house mice and their reciprocal hybrids. , 1994, The American journal of physiology.

[65]  G. Diffee,et al.  Effects of endurance exercise on isomyosin patterns in fast- and slow-twitch skeletal muscles. , 1990, Journal of applied physiology.

[66]  T. Garland,et al.  Maximal sprint speeds and muscle fiber composition of wild and laboratory house mice , 1995, Physiology & Behavior.

[67]  R. Fitts,et al.  Effect of swim exercise training on human muscle fiber function. , 1989, Journal of applied physiology.

[68]  R. Fitts,et al.  Muscle Mechanics: Adaptations with Exercise‐Training , 1996, Exercise and sport sciences reviews.

[69]  W. Malaisse,et al.  Interaction of branched chain amino acids and keto acids upon pancreatic islet metabolism and insulin secretion. , 1980, The Journal of biological chemistry.