Department of Kinesiology, University of Waterloo, Waterloo, Ontario, Canada N2L 3G1; The Karolinska Institute, S-141 Stockholm 86, Sweden; and Department of Medicine, McMaster University Medical Centre, Hamilton, Ontario, Canada L8N 3Z5
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ABSTRACT |
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We examined the effects of increasing a known
lactate transporter protein, monocarboxylate transporter 1 (MCT1), on
lactate extrusion from human skeletal muscle during exercise. Before
and after short-term bicycle ergometry training [2 h/day, 7 days
at 65% maximal oxygen consumption
(O2 max)],
subjects (n = 7) completed a
continuous bicycle ergometer ride at 30%
O2 max (15 min), 60%
O2 max (15 min), and
75%
O2 max (15 min).
Muscle biopsy samples (vastus lateralis) and arterial and femoral
venous blood samples were obtained before exercise and at the end of
each workload. After 7 days of training the MCT1 content in muscle was
increased (+18%; P < 0.05). The concentrations of both muscle lactate and femoral venous
lactate were reduced during exercise
(P < 0.05) that was performed after
training. High correlations were observed between muscle lactate and
venous lactate before training (r = 0.92, P < 0.05) and after training
(r = 0.85, P < 0.05), but the slopes of the
regression lines between these variables differed markedly. Before
training, the slope was 0.12 ± 0.01 mM
lactate · mmol
lactate
1 · kg
muscle dry wt
1, and this
was increased by 33% after training to 0.18 ± 0.02 mM
lactate · mmol
lactate
1 · kg
muscle dry wt
1. This
indicated that after training the femoral venous lactate concentrations
were increased for a given amount of muscle lactate. These results
suggest that lactate extrusion from exercising muscles is increased
after training, and this may be associated with the increase in
skeletal muscle MCT1.
glycogen; exercise; muscle lactate; femoral venous lactate; arteriovenous difference
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INTRODUCTION |
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THE FUNCTIONAL ROLE of monocarboxylate transporter 1 (MCT1) in muscle has not been established fully. The presence of MCT1 in rodent heart and oxidative skeletal muscles (10) suggested that its function would be to import lactate from the circulation into the cell where it could be oxidized. We have recently shown that MCT1 content is highly related to the oxidative muscle fiber content of rat skeletal muscles, their heart-type lactate dehydrogenase content and citrate synthase activities (22). All these relationships point very strongly to the fact that MCT1 is important for the removal of lactate from the circulation. These observations support recent studies in which lactate transport into oxidative muscles was greater than into glycolytic muscles (6, 18). In early studies in humans, it was also shown that lactate uptake after exercise was correlated with the presence of slow-twitch oxidative fibers (5), which are presumably high in MCT1 content. Thus the first important step to facilitate lactate uptake into the muscle cell appears to reside at the level of MCT1, although lactate uptake may not be the only function of this monocarboxylate transporter.
MCT1 may also facilitate the extrusion of lactate from muscle. There is some evidence for this suggestion. Studies in our laboratory have shown that lactate efflux from sarcolemmal vesicles is increased (20) under conditions in which MCT1 is also known to be increased (21). This begins to suggest a second physiological role for MCT1, namely, to assist with the elimination of lactate from exercising muscles. Indeed, in Ehrlich-Lettre tumor cells, which produce prodigious quantities of lactate, MCT1 is abundantly expressed (7) and its role is very clearly one of facilitating the extrusion of lactate. Thus muscles enriched with MCT1 are able to take more lactate from the circulation (1, 22) and they can also extrude more of this metabolite from the muscle (20, 21).
To examine whether lactate extrusion from muscle was increased when MCT1 in muscle was increased we compared the relationship between leg muscle lactate with femoral venous lactate before and after training, and we measured skeletal muscle MCT1 before and after training. We hypothesized that, when the MCT1 content of muscle is increased, the venous lactate will be higher for a given amount of intramuscular lactate.
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METHODS |
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Seven young males participated in these experiments (ages 23.4 ± 1.5 yr; height 181 ± 2 cm; weight 81.1 ± 4.1 kg). Ethical approval was obtained before the studies were undertaken, and informed consent was obtained from each subject.
Subjects trained for 7 (n = 5) or 8 (n = 2) days for 2 h/day at 60%
maximal oxygen consumption
(O2 max) on a bicycle
ergometer. Two days before training commenced and one day after
training was completed, each subject (not fasted) participated in a
standardized test consisting of continuous, progressive bicycle
ergometer exercise at 30%
O2 max (15 min), 65%
O2 max (15 min), and 75%
O2 max (15 min). The
femoral vein was catheterized percutaneously using the Seldinger
technique after administration of 3-4 ml of xylocaine without
epinephrine, as described elsewhere (4). The brachial artery was
catheterized percutaneously with a radiopaque Teflon catheter after
local anesthesia with 0.5 ml of xylocaine without epinephrine (4).
Before each test and at the end of each workload, muscle biopsies were
obtained from the vastus lateralis as previously described (3). Femoral
venous and arterial blood samples were obtained midway through each
exercise bout and just before the muscle biopsy sample. Blood samples
were analyzed for lactate (2), and muscle samples were analyzed for
lactate and glycogen as previously described (13). Muscles samples
(~50 mg) were analyzed for MCT1 content using Western blotting (22).
Because these blood lactate concentrations were almost identical in
every instance, they were averaged for each workload.
Sample preparation for Western blotting.
Proteins were isolated from muscles for Western blotting as previously
described (22). Briefly, muscles (~50 mg) were homogenized in 2 ml of
buffer
A (210 mM sucrose, 2 mM ethylene
glycol-bis(-aminoethyl ether)-N,N,N',N'-tetraacetic
acid, 40 mM NaCl, 30 mM
N-2-hydroxyethylpiperazine-N'-2-ethanesulfonic acid, 5 mM EDTA, and 2 mM phenylmethylsulfonyl fluoride, pH 7.4) for
two interrupted 15-s bursts with a polytron homogenizer set at 8. Homogenates were transferred to centrifuge tubes, and 2 ml of
buffer A, used to rinse the polytron,
were added to these tubes. Then 3 ml of
buffer
B (1.167 M KCl, 58.3 mM tetrasodium pyrophosphate) were added, mixed briefly, and then set on ice for 15 min. After centrifugation at 230,000 g
for 75 min at 4°C, the supernatant fluid was discarded and the
pellet was washed thoroughly with 1-2 ml of
buffer
C [10 mM
tris(hydroxymethyl)aminomethane (Tris)-base, 1 mM EDTA, pH 7.4].
The pellet was resuspended in 600 µl of
buffer
C and homogenized for two interupted
10-s bursts with a polytron set at 7. Then 200 µl of 16% sodium
dodecyl sulfate (SDS) were added and samples were removed from ice,
vortex mixed, and centrifuged at 1,100 g for 20 min at room temperature. The supernatant was divided into aliquots and stored at
80°C for protein assay and immunoblot detection of MCT1.
Western blotting of MCT1. A polyclonal antipeptide antibody (gift from Dr. A. P. Halestrap and Dr. R. C. Poole, Department of Biochemistry, University of Bristol) directed against the putative 11th and 12th loop of MCT1 was produced by immunizing New Zealand White rabbits with a synthetic peptide. This antibody was raised and affinity purified as described elsewhere (7). The polyclonal antibody yielded a single band on a Western blot that corresponded to a molecular mass of ~43 kDa, consistent with that reported for MCT1 (9, 10).
Protein samples of the muscles and prestained molecular weight markers (Bio-Rad) were separated on 12% SDS-polyacrylamide gels (150 V for 1 h). Proteins were then transferred from the gel to immobilon polyvinylidene difluoride membranes (100 V, 90 min). Membranes were incubated on a shaker overnight (~16 h) in buffer D [20 mM Tris-base, 137 mM NaCl, 0.1 M HCl (pH 7.5), 0.1% (vol/vol) Tween 20, and 10% (wt/vol) nonfat dried milk] at room temperature. Membranes were then incubated with diluted MCT1 antibody (1:500) in buffer D for 2 h, followed by three washes in buffer E (i.e., buffer D without dried milk: 15-min wash, and 2 × 5-min washes) followed by incubation for 1 h with donkey anti-rabbit immunoglobulin G horseradish peroxidase-conjugated secondary antibody (1:3,000, Amersham, NA 934) in buffer E. Membranes were washed as before with buffer E. Thereafter, MCT1 was detected with the use of an enhanced chemiluminescence (ECL) detection method by exposing the membranes to film (Hyperfilm-ECL; Amersham) at room temperature according to the instructions of the manufacturer (Amersham). Film was developed in developer (Kodak) and fixed in GBX fixer-replenisher (Kodak). The intensity of the resulting bands on the immobilon membrane was quantitated using a scanner (Abaton) and a Macintosh LC computer with appropriate software (Scan Analysis, Biosoft, Cambridge, UK). The increase in MCT1 was calculated as follows: %increase = [(posttraining MCT1/pretraining MCT1) × 100] ![]() |
RESULTS |
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The short-term training did not increase
O2 max (pretraining
3.66 ± 0.20 l/min; posttraining 3.76 ± 0.25 l/min;
P > 0.05). This is consistent with
our previous work in which we used this type of short-term aerobic
training procedure (8, 28).
Glycogen.
After training, the glycogen concentrations were increased at rest by
35% (pretraining 472 ± 28 mmol/kg dry wt; posttraining 638 ± 73 mmol/kg dry wt; P < 0.05). In
total 52% of the muscle glycogen was used during exercise when
subjects were untrained, whereas after training only 32% of the
available muscle glycogen pool was used. However, absolute changes ( mmol · kg dry
wt
1 · 15 min
1) in the rates of
muscle glycogen utilization before and after training did not differ
between respective work bouts at 30 and 65%
O2 max
(P > 0.05). Less glycogen was used
during the heaviest exercise bout (75%
O2 max) after subjects
were trained (pretraining:
glycogen from end
of exercise at 65%
O2 max to end of
exercise at 75%
O2 max = 129.5 ± 25.6 mmol · kg dry
wt
1 · 15 min
1 at 75%
O2 max; posttraining:
glycogen from end of exercise at 65%
O2 max to end of
exercise at
75%
O2 max = 56.5 ± 23.9 mmol · kg dry
wt
1 · 15 min
1 at 75%
O2 max;
P = 0.06; Fig.
1).
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MCT1. By using Western blotting, with an antibody to the MCT1 protein, we were able to measure MCT1 in human muscle (Fig. 2). After training, the MCT1 content in muscle samples was significantly increased. The mean increase after 7 days of training was 18% (range 0 to +62%; Fig. 2; P < 0.05).
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Lactate. Repeated-measures analyses of variance were used to compare the lactate responses before and after training. In general, after the 7-day training period, 1) the concentrations of arterial and femoral venous lactate were reduced during exercise (P < 0.05; Fig. 3), 2) the arteriovenous lactate differences were reduced during exercise (P < 0.05; Fig. 4), and 3) the concentrations of muscle lactate were reduced during exercise (P < 0.05; Fig. 5).
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DISCUSSION |
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This is the first study to show that MCT1 content in human skeletal muscle can be increased with a period of intense short-term training. These observations parallel studies with rodents in which MCT1 was increased after a brief period of chronic electrical stimulation of skeletal muscles (21) and after 5 days of treadmill training (1). We have previously reported that glucose transporter proteins were increased in humans with a short-term training program (28).
We also observed that the femoral venous lactate concentrations were greater for a given muscle lactate concentration after training. The greater range of lactate concentrations in muscle before training (Fig. 4) did not influence these observations. The slope of the regression line between muscle lactate and venous lactate was almost the same, whether we used all of the pretraining data or whether the pretraining data were restricted to the same muscle lactate range observed after training. Thus our study suggests that the rate of lactate extrusion from human skeletal muscle may be increased with training.
When the data were compared at each of the exercise workloads before and after training (Figs. 3-5), the typical reductions in muscle and blood lactate concentrations were observed that have been reported in many previous studies with exercise training. Reductions in arteriovenous lactate concentrations were observed (Fig. 4). This, however, could be due to the concomitant reductions in arterial lactate and muscle lactate that occurred with training. The small arteriovenous difference after training could be taken to indicate that both lactate uptake and release were enhanced with training. The present data do not allow us to examine if lactate uptake by muscle was increased, since muscle lactate is the result of lactate taken up by muscle and lactate produced within the muscle at the same time. In contrast, when comparing the relationship between muscle lactate and venous lactate measured at the same time, one obtains a rough index of muscle lactate efflux.
If lactate extrusion from muscle is indeed increased with training, this could be due in part to the increase in MCT1 content in the trained muscle. We have data indicating that MCT1 is found on the surface of skeletal muscle and is not found in intracellular sites within muscles (23). Thus translocation of this transport protein is not a likely consideration in our studies. The training-induced increase in MCT1 was modest and was likely confined to the surface of the muscle. However, a small change in a transport protein can still be physiologically important. In previous studies we have shown that increments or decrements of ~10% of the glucose transporter proteins GLUT-4 or GLUT-1 are associated with small changes in insulin-stimulated glucose transport (12, 26, 27), respectively. Thus the increase in MCT1 in the present study is presumably also physiologically significant. In particular, the increase in MCT1 could have facilitated the increased extrusion of lactate from the muscle suggested by our data.
Although we did not measure lactate transport directly, our results may be interpreted in the context of a change in lactate transport by skeletal muscle plasma membranes. There is good evidence that lactate transport across the sarcolemmal membrane is increased with training (1, 24, 30) and with chronic muscle stimulation (20, 21) in rats. Lactate transport is also greater in well-trained humans (29). In other studies we have associated the increased lactate movement across the sarcolemmal membrane with an increased content of MCT1 after training (1) and after a period of chronic muscle stimulation (21). When MCT1 is over-expressed in Chinese hamster ovary cells, lactate uptake is increased (32) and MCT1 assists with the extrusion of lactate from cells that produce prodigious quantities of lactate (i.e., Ehrlich-Lettre tumor cells) (7). Therefore, it is possible that the training-induced increase in femoral venous lactate for a given amount of leg muscle lactate is associated with the observed increase in muscle MCT1.
The suggestion from the present studies that MCT1 could facilitate the extrusion of lactate out of the muscle is not necessarily at odds with MCT1's role in facilitating the removal of lactate from blood (22). It seems that MCT1 may contribute to enhancing both lactate influx and efflux. Muscles with more MCT1 can take up more lactate from the circulation (1, 21, 22). The direction of lactate flux (uptake or extrusion) is governed largely by the lactate concentration gradient across the sarcolemma (cf. Ref. 15). However, during exercise it is advantageous to extrude lactate from the exercising muscles to limit reductions in muscle pH. It may be that the same transporter facilitates lactate influx into and efflux out of this tissue, since lactate transport across the skeletal muscle sarcolemma is apparently symmetrical (17). In our own studies, lactate movement either into (21) or out of skeletal muscle (22) has been observed in rat muscles when MCT1 content had been increased via chronic electrical stimulation in these muscles.
We cannot be entirely certain that our observations are completely attributable to MCT1. There is considerable suspicion that there may be a family of MCT proteins, but only MCT1, MCT2, and MCT3 have been cloned. The kinetic characteristics of MCT1 and MCT2 are similar for lactate, but a fourfold lower Michaelis constant for pyruvate was observed for MCT2 compared with MCT1 (9). In rats we have not been able to detect MCT2 in muscle, only in liver (Bonen, unpublished data). MCT3 has been identified in chick retinal pigment epithelium, but MCT3 is not expressed in other tissues (33). Other MCT transporter isoforms might also be present in skeletal muscles, particularly in white muscles in which transport is also observed (15) despite a very low content of MCT1 (21, 22). Thus a transporter to cope with lactate transport in white muscle would seem to exist, although such an MCT has not yet been reported. It is possible that training could have increased the hypothetical "white muscle" MCT transporter, but, until such an MCT isoform is discovered, we can only base our explanation on MCT1, which is known to exist in skeletal muscles (1, 21, 22) and which is increased by exercise training (1) and chronic muscle stimulation (21).
In summary, we have shown that, after a period of short-term training, MCT1 content is increased in skeletal muscles. After training, the lactate concentrations in muscle and blood were reduced during a standardized exercise bout. However, for a given lactate concentration in leg muscle, femoral venous lactate concentrations were increased after training. We interpret these observations to mean that with exercise training lactate extrusion from muscle is increased and that this may possibly be attributable to the observed increase in MCT1.
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ACKNOWLEDGEMENTS |
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We thank T. Bragg, G. Obminski, M. Hollidge-Horvatt, Dr. M. Ganagaragah, and Dr. D. R. McConachie for technical assistance. We thank Dr. A. P. Halestrap and Dr. R. C. Poole, Department of Biochemistry, University of Bristol, Bristol, UK for providing us with the MCT1 antibody.
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FOOTNOTES |
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These studies were supported by the Natural Sciences and Engineering Research Council of Canada and the Medical Research Council of Canada.
C. T. Putman was supported by a Medical Research Council of Canada Studentship. G. J. F. Heigenhauser was a career investigator of the Heart and Stroke Foundation of Ontario.
Address for reprint requests: A. Bonen, Dept. of Kinesiology, Univ. of Waterloo, Waterloo, ON, Canada N2L 3G1.
Received 29 April 1997; accepted in final form 1 October 1997.
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