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Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions

Aerobic Exercise Training Increases Skeletal Muscle Protein Turnover in Healthy Adults at Rest^1,2

Matthew A. Pikosky^*, Patricia C. Gaine^*, William F. Martin^*, Kimberly C. Grabarz^*, Arny A. Ferrando, Robert R. Wolfe and Nancy R. Rodriguez^*,3

^* Department Nutritional Sciences, University of Connecticut, Storrs, CT and Department of Surgery, University of Texas Medical Branch, Galveston, TX

³ To whom correspondence should be addressed. E-mail: nancy.rodriguez{at}uconn.edu.

	ABSTRACT

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The effect of a 4-wk aerobic exercise training program (30–45 min, 3–5 d/wk, 65% maximal heart rate) on mixed skeletal muscle protein fractional synthetic rate (FSR), fractional breakdown rate (FBR), and net protein balance (FSR – FBR) (NET) was examined in 8 healthy, previously unfit men and women [21.0 ± 0.4 y, 163.7 ± 4.4 cm, 75.6 ± 5.7 kg, 33.5 ± 4.1% body fat, VO_2peak 38.6 ± 2.3 mL/(kg·min)] fed eucaloric diets providing 0.85 g protein/(kg·d) for the 6-wk study. Measurements were made at baseline after 2 wk of diet intervention only, and after 4 wk of aerobic exercise training and diet intervention. Primed continuous infusions of ring-[²H₅]-phenylalanine (2 µmol/kg; 0.05 µmol/(kg·min) and [¹⁵N]-phenylalanine (2 µmol/kg; 0.05 µmol/(kg·min) were used to assess skeletal muscle protein turnover at rest via the precursor-product method. Endurance training improved cardiovascular fitness, with a significant increase in VO_2peak (P < 0.01) and a significant decrease in running time on a standard course (P < 0.01). There were no significant changes in body mass or composition. There was a significant increase in FSR (0.077 ± 0.007 vs. 0.089 ± 0.006%/h, P < 0.05) and decrease in NET (FSR – FBR) (–0.023 ± 0.004 vs. –0.072 ± 0.012%/h, P < 0.05); FBR tended to increase (0.105 ± 0.014 vs. 0.143 ± 0.018%/h; P = 0.06) after training. Findings show that aerobic training for 4 wk increases skeletal muscle protein turnover in previously unfit subjects.

KEY WORDS: • phenylalanine • endurance exercise • skeletal muscle protein turnover

Exercise has a profound effect on protein metabolism. Of particular interest is the influence that exercise has on skeletal muscle protein turnover (SMPTO)⁴, given that skeletal muscle comprises 40% of all body protein stores (1). The magnitude and direction by which exercise influences SMPTO are affected by a variety of factors including the mode, intensity, and duration of the exercise performed, as well as the training state of the individual. Although the SMPTO response to resistance training has been clearly established, much less is known about endurance exercise. After resistance exercise, there is a significant increase in the rates of both mixed muscle fractional synthesis (FSR) and breakdown (FBR) (2–5) . The magnitude and duration of the increase in synthesis exceed that of breakdown, resulting in an improved net muscle protein balance after resistance exercise. However, in the fasted state, net balance remains negative until nutrients are provided (6–12).

The effect of endurance exercise on SMPTO is far less clear. To date, only 3 studies have examined FSR after endurance exercise in fasting humans (13–15). Carraro et al. (14) and Sheffield-Moore et al. (13) both found increases in FSR after treadmill walking at 40% VO_{2 max}. A high intensity swimming workout employed by Tipton et al. (15) resulted in a 41% increase in FSR; however, this effect was not significant. It is difficult to draw definitive conclusions from only 3 studies that differ greatly in design. However, collectively, these findings suggest that FSR increases after acute endurance exercise.

Although there is not a consensus concerning the influence of an acute exercise bout on SMPTO, even less is known about the influence of chronic aerobic training. Because exercise generally lasts for a relatively short period of time relative to time spent not exercising, studying SMPTO at rest may be of greater value to our understanding of the influence of chronic aerobic training on SMPTO. To date, only one study has examined the effect of chronic aerobic exercise training on mixed skeletal muscle FSR. In that study, 4 mo of cycling resulted in a 22% increase in FSR in fasted individuals at rest (16). Although that investigation provided novel findings about the synthetic response in muscle to aerobic exercise training, rates of breakdown were not determined. Rates of synthesis and breakdown are necessary for complete characterization of SMPTO and will better define the effect of endurance exercise on protein metabolism.

The present investigation employed the measurement of rates of both protein synthesis and breakdown to determine how aerobic exercise training influenced skeletal muscle protein turnover at rest. Subjects in this study were previously untrained, healthy men and women. To minimize the influence of diet (specifically variations in energy and protein intake), subjects consumed a eucaloric diet providing a constant level of protein throughout the 6-wk intervention. This study is unique because it assesses the effect of aerobic exercise training on both FSR and FBR in human skeletal muscle during a period for which dietary control was implemented. We tested the hypothesis that a 4-wk aerobic training program would result in an upregulation in skeletal muscle protein turnover as indicated by increases in both FSR and FBR. The findings of the present study will allow for more complete comparisons regarding the effect of training mode on SMPTO and provide a foundation for future studies examining the effect of nutritional supplementation with endurance exercise on SMPTO.

	SUBJECTS AND METHODS

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
    Experimental design. Untrained apparently healthy men (n = 4) and women (n = 4) participated in a 6-wk diet and exercise intervention study. After a 2-wk dietary adjustment period during which subjects consumed a standardized diet, they undertook a 4-wk aerobic exercise training program. Subjects consumed the standardized diet throughout the 6-wk exercise intervention period. Stable isotope methodology and muscle biopsies were used to assess skeletal muscle protein turnover at baseline, after 2 wk of diet alone (Untrained), and after 4 wk of an aerobic exercise training program (Trained).

    Subjects. Following project approval by the Institution Review Board at the University of Connecticut, individuals aged 18–25 y were recruited from the University community. Before selection for the study, participants were asked to provide a complete medical history, activity log, and a record of dietary intake. Exclusion criteria included the following: 1) exercising >90 min/wk, 2) men and women with VO_2peak values 45 mL/(kg·min) and 40 mL/(kg·min), respectively (17), 3) reporting of any metabolic or cardiovascular abnormalities (i.e., irregular heartbeats, high blood pressure), gastrointestinal disorders (i.e., specific food allergies), and 4) use of any nutritional/sports supplements or anabolic steroids. Women were eumenorrheic and not pregnant as determined by self-report. Informed, written consent was obtained from all subjects.

    Diet and exercise intervention. Once energy needs were determined, protein intakes were set at a goal intake of 0.8 g/(kg body weight·d). Macronutrient intakes as percentages of total dietary energy were 60% carbohydrate, 10% protein, and 30% fat. Energy intake was adjusted to meet the increased energy requirements of subjects throughout the exercise-training period for weight maintenance. All meals were provided for study participants for the duration of the 6-wk study and study personnel were present at meals to weigh and serve the appropriate portions of food to each subject. Daily dietary records were analyzed for energy and macronutrient composition using Nutritionist Pro Software^TM (First Data Bank, Version 1.1). The 4-wk aerobic training program included supervised and monitored exercise sessions consisting of stretching and group run/walk set at a pace to elicit 65–85% of age-predicted max heart rate, 3–5 d/wk, for 30–45 min/session as described previously (18).

    Additional measurements. Body weight and height were measured using a balance beam scale equipped with a measuring rod (Health-o-meter). Body weight was assessed at baseline and twice weekly throughout the study to ensure body weight maintenance. Body composition was assessed via dual-energy X-ray absorptiometry (DPX-MD Lunar). Measurements were made at baseline (Untrained) and after 4 wk of exercise training (Trained).

Maximal graded exercise tests were conducted before and after the 4-wk aerobic exercise training program. VO_2peak was determined via an indirect open circuit respiratory system (MedGraphics CPX/D, Medical Graphics) on a treadmill (Quinton MedTrack ST55) (19).

    Plasma amino acids. Plasma amino acid concentrations were determined using HPLC (Dionex Laboratories) and postcolumn ninhydrin detection (Pickering Laboratories) with an internal standard (norleucine).

    Determination of skeletal muscle protein turnover. Mixed muscle protein FSR and FBR were assessed at rest at baseline (Untrained) and after 4 wk of endurance training (Trained). These measurements were performed 36–40 h after the completion of each subject's last training session, run time trial, and VO_2peak.

On study days, subjects arrived at the Metabolic Assessment Laboratory at the University of Connecticut between 0600 and 0700 after an overnight fast. A 20-gauge Teflon catheter (4.45 cm, Jelco/Critikon) was inserted into an antecubital vein to obtain a background blood sample and for subsequent isotope infusions (Fig. 1). After the collection of the baseline blood sample, a primed, continuous infusion [2 µmol/kg; 0.05 µmol/(kg·min) Cambridge Isotope] of ring-[²H₅]-phenylalanine was initiated (0 min) and maintained throughout the protocols for determination of FSR. Another catheter (3.18 cm) was placed in a hand vein contralateral to the infusion for blood sampling. At 120 min, participants were prepped under sterile conditions for a muscle biopsy that was taken from the lateral portion of the vastus lateralis (20 cm above the knee) as described previously (20).

View larger version (14K): [in this window] [in a new window]   FIGURE 1  A schematic depicting the infusion/muscle biopsy protocol in 8 healthy men and women who underwent 2 wk of dietary intervention and 4 wk of aerobic exercise training and dietary intervention. After baseline blood collection for the determination of [2H5]- and [15N]-phenylalanine background enrichment, the [2H5]-phenylalanine isotope infusion was initiated. The first muscle sample was obtained at 120 min; the [15N]-phenylalanine infusion was then initiated. Subsequent muscle sampling occurred at 380 and 300 min. Blood draws were taken at regular time points as indicated by the stars.

    Blood and muscle enrichments. Blood samples obtained from the heated arterialized hand vein for determination of phenylalanine enrichments (22) were immediately precipitated in tubes containing 15% sulfosalicyclic acid and thoroughly mixed. The whole blood samples were centrifuged (6000 x g) and the supernatant was frozen at –80°C until future analysis. The muscle tissue sample was immediately blotted dry; any visible fat or connective tissue was removed, and the sample was frozen in liquid nitrogen. Samples were then stored at –80°C until future processing. [²H₅]- and [¹⁵N]-phenylalanine enrichments in blood and in bound and intracellular muscle were determined according to previously described methods (2,20).

    SMPTO calculations. FSR was calculated using the direct incorporation method (2,20,23) based on the rate of [²H₅]-phenylalanine tracer incorporation from muscle intracellular fluid into bound skeletal muscle protein between muscle samples at 120 and 300 min. FBR was calculated using the tracee release method previously described by Zhang et al. (21), which is based on the dilution of plasma and intracellular muscle [¹⁵N]-phenylalanine enrichments from the release of unlabeled phenylalanine from bound muscle protein. FBR was calculated from the decay of enrichments of these 2 pools once the [¹⁵N]-phenylalanine infusion was terminated at 240 min of the protocol. Because no muscle biopsy was taken at the [¹⁵N]-phenylalanine plateau, this plateau was calculated by using the ratio of the mean intracellular ring-[²H₅]-phenylalanine to arterialized ring-[²H₅]-phenylalanine enrichment and multiplying by the arterialized [¹⁵N]-phenylalanine enrichment (2). This calculation was shown to correlate with direct measurements of the intracellular [¹⁵N]-phenylalanine enrichment determined via skeletal muscle biopsy at plateau (r = 0.97, P < 0.001) (3).

    Statistical analysis. Primary outcome measures were skeletal muscle FSR, FBR, and NET at baseline (Untrained) and after training (Trained). Means were compared using a paired Student's t test. Differences were considered significant at P < 0.05. Because no gender differences were noted, data for men and women were combined and presented as a single group. Values in the text are means ± SEM.

	RESULTS

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
    Subject characteristics. Body mass and composition did not change after 4 wk of training (Table 1). REE and VO_2peak increased significantly post-training and time trial performance improved compared with pretraining values (P < 0.01).

    Plasma amino acids. Fasting plasma leucine concentrations decreased significantly, whereas valine increased from baseline after 4 wk of training (P < 0.05) (Table 2). In addition, total branched-chain amino acids (BCAA), total essential amino acids (EAA), and total nonessential amino acids (NEAA) all decreased (P < 0.05) in these fasting subjects at rest after 4 wk of endurance exercise training.

View larger version (12K): [in this window] [in a new window]   FIGURE 2  Plasma (A) and Muscle (B) [15N]- and [2H5] phenylalanine enrichments (tracer/Tracee) in 8 healthy men and women who underwent 2 wk of dietary intervention and 4 wk of aerobic exercise training and dietary intervention at baseline (Untrained) and after the aerobic training (Trained). Values are means ± SEM.

View larger version (9K): [in this window] [in a new window]   FIGURE 3  Mixed-muscle FSR, FBR, and NET in 8 healthy men and women who underwent 2 wk of dietary intervention and 4 wk of aerobic exercise training and dietary intervention at baseline (Untrained) and after the training (Trained). Values are means ± SEM. *Different from Untrained, P < 0.05.

	DISCUSSION

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Research examining the response of skeletal muscle protein metabolism to aerobic exercise training is limited. A recent study by Short et al. (16) provides the only other data regarding skeletal muscle protein metabolism after aerobic exercise training in human volunteers. These investigators observed a 22% increase in FSR at rest, after 4 mo of aerobic training in previously untrained subjects. This is consistent with the present investigation in which FSR increased 17% at rest after 4 wk of aerobic training. Although the subjects in the Short study encompassed a greater age range (19–87 y) than that of the present study (18–25 y), similar improvements in VO_2peak were documented from pre- to post-training (9.5 vs. 8.4% for the Short study vs. present study, respectively).

The increase in FSR after endurance training noted in these studies may in large part reflect an increased synthesis of proteins responsible for bringing about the adaptations associated with this mode of exercise [i.e., increased mitochondrial volume (24), mitochondrial enzyme activity (25), capillary to muscle fiber ratio, capillary density, and the number of capillaries around a given muscle fiber (25)]. Although we do not have data supporting this hypothesis, Short et al. (26) found increased glucose transporter (GLUT)-4 mRNA and GLUT-4 protein levels after training, and mitochondrial biogenesis was evident from increases of mitochondrial enzymes and mitochondrial protein mRNA. Furthermore, the increase in mixed muscle synthetic rates was not paralleled by changes in fat-free mass or leg muscle size (26).

The addition of FBR in the current study provides further insight into the effects of aerobic exercise training on skeletal muscle protein turnover because it enables the calculation of NET protein balance (FSR – FBR). Until now, this had not been determined at rest after an aerobic training program. FBR tended to increase (P = 0.06), ultimately resulting in a more negative NET balance after the 4-wk training program.

A negative NET is expected in fasting subjects, where rates of breakdown exceed those of synthesis in the absence of exogenous amino acids (8). However, the finding of a more negative NET after endurance training differs from what is observed after resistance exercise. A single bout of resistance exercise results in improved NET balance because rates of synthesis are elevated by a greater magnitude and for a longer duration than rates of breakdown (10).

The catabolic environment observed acutely in the present study may not be representative of the 24-h skeletal muscle protein turnover response after aerobic training. Attempting to quantify or extend the effect of this observed NET balance, assessed over a 3-h time period in a fasting state, on lean body mass in the long term would be an oversimplification of protein turnover. As discussed by Phillips et al. (27), the maintenance of lean body mass over the course of a day is due to a fluctuation between the gains and losses of muscle proteins in response to feeding and fasting. Therefore, in the present study, although net balance was more negative after training in the fasted state, it is likely that there was a compensatory positive net muscle protein balance in response to feeding because no changes were noted in body composition and or body mass throughout the 4-wk training period. This notion is supported by multiple studies in which a shift to a positive net balance occurs following feeding after resistance (6,8–10) and endurance (28) exercise.

In the current investigation, plasma BCAA, EAA, and NEAA concentrations declined in response to 4 wk of aerobic exercise training. It is unlikely that there was an increased use of amino acids for fuel because both leucine oxidation and total protein oxidation decreased at rest after training (19). Because changes in circulating amino acid levels do not necessarily reflect intracellular amino acid availability, the physiological significance of these small differences in the context of the changes noted in skeletal muscle protein turnover must be viewed cautiously.

Our findings of a more negative NET balance and a decrease in plasma amino acid concentrations after training suggest that the protein intake of 0.85 g/kg body weight consumed throughout the investigation may have been less than optimal in our exercising subjects despite their adequate energy intakes. A substantial amount of research showed that individuals who participate in routine aerobic training likely have protein needs in excess of the current RDA for protein (20,29–32). However, it should be noted that there are some that refute this notion (33,34), especially in situations in which energy intake is sufficient to meet the demands of exercise (34,35). Furthermore, Levenhagen et al. (28) examined nutritional supplementation after endurance exercise and concluded that amino acid rather than energy availability was more important for postexercise repair and synthesis of muscle proteins. Perhaps if subjects had consumed a greater level of protein in the current study, free amino acid pools would have expanded, thereby limiting the need for amino acids derived from endogenous sources and attenuating protein breakdown. In a recent study from our laboratory, we in fact demonstrated that variation in protein intake can augment amino acid pools, resulting in changes in FSR after endurance exercise (20).

The findings of the present investigation suggest an upregulation of skeletal muscle protein turnover in response to aerobic exercise training. Given that maintenance of energy balance was a focal point in the current study, the resulting negative NET balance can be attributed to either aerobic training, inadequate level of protein intake, or a combination of both. These findings provide support for future investigations evaluating both FSR and FBR at rest in response to endurance exercise at varying levels of dietary protein to characterize further the skeletal muscle protein metabolic response to this mode of training.

	FOOTNOTES

 
¹ Presented in abstract form at Experimental Biology 03, April 2003, San Diego, CA [Pikosky MA, Gaine PC, Martin WF, Maresh CM, Ferrando AA, Wolfe RR, Rodriguez NR. Endurance training affects muscle protein synthesis at rest in previously unfit men and women (abstract). FASEB J. 2003;17(5):524.1].

² Supported by the American Egg Board.

⁴ Abbreviations used: BCAA, branched-chain amino acids; EAA, essential amino acids; NEAA, nonessential amino acids; FSR, fractional synthetic rate; FBR, fractional breakdown rate; GLUT, glucose transporter; NET, net protein balance (FSR – FBR); PCA, perchloric acid; SMPTO, skeletal muscle protein turnover; VO_2peak, peak oxygen uptake.

Manuscript received 5 August 2005. Initial review completed 31 August 2005. Revision accepted 29 October 2005.

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