Lactate availability is not the major factor limiting muscle glycogen repletion during recovery from an intense sprint in previously active fasted rats
1 School of Human Movement and Exercise Science, University of Western
Australia, Crawley, Western Australia, Australia, 6009
2 Department of Biochemistry and Molecular Biology, James Cook University,
Townsville, Queensland, Australia, 4811
* Author for correspondence (e-mail: fournier{at}cyllene.uwa.edu.au)
Accepted 12 October 2004
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Summary |
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Key words: carbohydrate, exercise, glycogen, glycogen synthase, muscle, recovery, regulation, rat
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Introduction |
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Given that, after a sprint, skeletal muscles have the capacity to replenish
their glycogen stores even without food intake, this raises the question of
what are the factors that limit the extent to which these stores are
replenished. Since the lactate accumulated during exercise is a major net
carbon source for the synthesis of muscle glycogen, it is generally assumed
that the extent of muscle glycogen repletion during recovery depends to some
extent on the proportion of accumulated lactate that is converted into
glycogen (Gaesser and Brooks,
1984; Gleeson,
1996
; Raja et al.,
2003
). Under conditions where an intense sprint effort is
supported primarily by the catabolism of muscle glycogen into lactate, the
conversion of all accumulated lactate and glycolytic intermediates into muscle
glycogen could result in the complete or near complete replenishment of muscle
glycogen stores. This could be the case for the animal species (e.g. fish,
amphibians, lizards) known to replenish completely their muscle glycogen
stores when recovering from an intense sprint effort
(Gratz and Hutchison, 1977
;
Gleeson, 1982
;
Milligan and Wood, 1986
;
Gleeson and Dalessio, 1989
;
Pagnotta and Milligan, 1991
;
Fournier and Guderley, 1992
;
Girard and Milligan, 1992
;
Scarabello et al., 1992
;
Gleeson, 1996
;
Milligan, 1996
;
Bräu et al., 1999
). In
contrast, the partial conversion of lactate into muscle glycogen in other
species, such as humans and rats, has been proposed to explain, in part, why
their muscle glycogen stores are only partially replenished after a sprint
(Hermansen and Vaage, 1977
;
Astrand et al., 1986
;
Hatta et al., 1988
;
Bangsbo et al., 1992
;
Choi et al., 1994
;
Nikolovski et al., 1996
;
Peters et al., 1996
;
Bangsbo et al., 1997
;
Ferreira et al., 2001
).
If, as predicted above, the amount of accumulated lactate is the primary
factor limiting the extent of muscle glycogen repletion post-intense exercise,
one would predict that under conditions where a large proportion of muscle
glycogen is oxidised by sustained moderate intensity exercise prior to a
sprint, only the glycogen converted to lactate (and to a lesser extent to the
glycolytic intermediates) during that sprint would be expected to be
replenished, thus leading to the partial replenishment of muscle glycogen.
Alternatively, skeletal muscles may possess critical minimal levels of
glycogen that are protected against sustained depletion, with the extent of
muscle glycogen repletion during recovery from an intense sprint effort in
fasted animals being determined primarily by the amount of glycogen required
to attain those protected levels, irrespective of lactate availability
(Raja et al., 2003). Which of
the above mentioned factors limits the extent of glycogen repletion
post-intense exercise is an important question that remains to be addressed.
For this reason, it is the primary objective of this study to adopt the above
mentioned rationale and examine whether the level of accumulated lactate is
the major factor determining the extent of glycogen repletion during recovery
from an intense sprint effort in fasted rats subjected to moderate intensity
exercise prior to the sprint.
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Materials and methods |
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Experimental animals
Adult male albino Wistar rats (280320 g) were obtained from the
Animal Resource Centre at Murdoch University, Western Australia. Male rats
were used in preference to females to avoid the physiological changes
associated with the oestrous cycle. The rats were kept at approximately
20°C on a 12 h:12 h L:D photoperiod and had unlimited access to water and
a standard laboratory chow diet (Glen Forrest Stockfeeders, Glen Forrest,
Western Australia 6071: 55% digestible carbohydrate, 19% protein, 5% lipid and
21% non-digestible residue by mass). Before experiments, the rats were fasted
for 24 h to deplete most of their stores of liver glycogen
(Ferreira et al., 2001) and to
prevent food present in the gut from providing carbon precursors for the
replenishment of muscle glycogen post-exercise. On the day of each experiment,
the animals were exercised and killed by cardiac excision between 9.00 and
12.00 h. The study was approved by the Animal Ethics Committee of the
University of Western Australia.
Exercise protocol
In order to test the hypothesis that lactate availability does not limit
the extent of muscle glycogen repletion post-intense exercise, groups of rats
were subjected to a combination of moderate and high intensity exercise. The
rationale for adopting such an exercise protocol to test our hypothesis has
already been described in the Introduction. Rats being natural swimmers, an
exercise protocol based on swimming was adopted in this study, the intensity
of the exercise being determined by the amount of lead weight attached to the
base of the tail (Ferreira et al.,
2001; Raja et al.,
2003
). The advantage of this exercise protocol over one that uses
a treadmill is that a prolonged training period is not required for the animal
to exercise at near maximal intensity. Another major strength of this exercise
protocol is that it results in highly reproducible changes in muscle glycogen
and lactate levels (Nikolovski et al.,
1996
; Ferreira et al.,
2001
). Prior to exercise, rats were weighed and a lead weight
equivalent to 0.5% body mass was attached to the base of the tail of each
animal. Each rat was then placed in a plastic tank (30 cm diameter, 48 cm
deep) filled with water at 34°C and forced to swim continuously for 30
min. A period of 30 min was chosen to prevent the complete aerobic depletion
of the stores of muscle glycogen during exercise. At the end of the 30 min
swim, some rats were sacrificed immediately, others had a lead weight
equivalent to 9.5% of body mass added to the base of their tails, and these
rats were made to swim for 3 min at high intensity as described previously
(Ferreira et al., 2001
).
Previous studies from this laboratory have shown that swimming with this
amount of lead weight results in a rapid and marked changes in muscle glycogen
and lactate levels (Nikolovski et al.,
1996
; Ferreira et al.,
2001
; Raja et al.,
2003
). Upon completion of the high intensity swim, the rats were
either killed immediately or allowed to recover individually in separate cages
without access to food for 30, 60 or 120 min. One group of rats served as the
non-exercised control group.
Tissue and blood sampling
Rats at rest or at 0, 30, 60 and 120 min during the post-exercise recovery
period were anaesthetised under halothane
(Ferreira et al., 1998) and
the following tissues were sampled: individual muscles (red gastrocnemius,
white gastrocnemius, mixed gastrocnemius and mixed quadriceps muscles), blood
by cardiac puncture and liver. The white, red and mixed gastrocnemius muscles
and mixed quadriceps muscle were selected because they are rich in fast twitch
white, fast twitch red fibres and a combination of both fibre types,
respectively (Maltin et al.,
1989
). These muscles were also selected because their glycogen
stores have been shown to be replenished from endogenous carbon sources during
recovery from high intensity exercise in fasted rats
(Ferreira et al., 2001
). After
removal, each muscle tissue was immediately freeze-clamped between aluminium
plates pre-cooled in liquid nitrogen, then wrapped in aluminium foil and
stored at 80°C. Blood was sampled from anaesthetised rats by
cardiac puncture using heparinised syringes and processed as described
below.
Extraction of blood and tissue metabolites
Immediately following removal from the heart, blood was transferred into an
heparinised Eppendorf microcentrifuge tube and centrifuged at 720
g for 5 min. After centrifugation, 100 µl of the plasma was
deproteinised in 900 µl of 6% (w/v) perchloric acid and centrifuged at 2000
g for 10 min; the remaining plasma was stored at
80°C. Following centrifugation, the supernatant was neutralised
with 2 mmol l1 K2CO3 and centrifuged
at 2000 g for 10 min. All samples were kept at 80°C
until analysis.
Prior to assay, muscles and liver were weighed and ground using a mortar
and pestle kept in liquid nitrogen, special care being taken to prevent the
tissues from thawing (Lehoux and Fournier,
1999). The powdered tissue was homogenised with 10 volumes of
ice-cold 6% (w/v) perchloric acid. A portion of the homogenate was used for
the determination of glycogen, whereas a 700 µl sample was centrifuged at
2000 g for 10 min, and the supernatant removed and kept on
ice. The pellet was re-extracted with 350 ml of 6% (w/v) perchloric acid
before recentrifugation at 2000 g for 10 min. Following
centrifugation, the two supernatants were combined, neutralised with 2 mmol
l1 K2CO3, and centrifuged before being
stored at 80°C until analysis. Glycogen, lactate, glucose and
glucose 6-phosphate were assayed as described by Bergmeyer and Gutmann
(Bergmeyer, 1974
).
Fractional velocity of glycogen synthase
Changes in the phosphorylation state of glycogen synthase can be estimated
indirectly by measuring its fractional velocity, which is defined as the ratio
of the enzyme activity in the presence of low and high levels of its
activator, glucose 6-phosphate (Bräu
et al., 1997). Since the phosphorylation of glycogen synthase
results in its inactivation when measured in the presence of low levels of
glucose 6-phosphate, it follows that the higher the phosphorylation state of
this enzyme, the lower its fractional velocity. The determination of the
fractional velocity of glycogen synthase was performed as described in recent
publications from this laboratory (James
et al., 1998
; Ferreira et al.,
2001
), using the filter paper method of Thomas et al.
(1968
). Briefly, muscles
previously weighed and ground were homogenised in the presence of 10 volumes
of glycerol buffer [50 mmol l1 Tris-HCl (pH 7.8 at
25°C), 100 mmol l1 KF, 10 mmol l1
EDTA, 60% (v/v) glycerol at 20°C]. After the addition of 10 volumes
of glycerol-free buffer [50 mmol l1 Tris-HCl (pH 7.8), 100
mmol l1 KF, 10 mmol l1 EDTA], the extracts
were re-homogenised for a further 30 s. The homogenates were centrifuged at
2000 g for 10 min, and the supernatants further diluted
fivefold with glycerol-free buffer before assay. The fractional velocity was
determined using an assay that consists of measuring the activity of the
enzyme at a sub-saturating near-physiological level of UDP-glucose (0.03 mmol
l1) in the presence of either low (0.1 mmol
l1) or high (5.0 mmol l1) glucose
6-phosphate concentrations (Bräu et
al., 1997
; James et al.,
1998
; Ferreira et al.,
2001
). Under these conditions, the reaction rates of glycogen
synthase in the presence of low or high glucose 6-phosphate levels were linear
with respect to both the amount of extract used and incubation time.
Expression of results and statistical analyses
All metabolite concentrations in tissues and plasma are expressed in
µmol g1 wet mass and mmol l1,
respectively. Glycogen synthase fractional velocities are expressed as a
percentage of maximal activity. Results are expressed as means ±
S.E.M. for nine rats. The effects of exercise and post-exercise
recovery on metabolite levels and enzyme activities were analysed with a
one-way ANOVA followed by Fisher LSD test using Stat View SE + Graphics
version 1.03 (Abacus Concepts, Berkeley, CA, USA,'88).
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Results |
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Prolonged exercise of moderate intensity resulted only in a small rise in muscle lactate levels (Fig. 2). In response to the sprint performed immediately afterwards, lactate levels increased significantly in all muscles examined (Fig. 2). During recovery, lactate returned to pre-exercise levels within 30 min and remained at low and stable levels thereafter (Fig. 2). In response to moderate intensity exercise, plasma lactate levels increased from 1.2±0.1 to 2.8±0.7 mmol l1, and increased further to 16.3±1.8 mmol l1 in response to the subsequent sprint. Within the following 30 min of recovery, plasma lactate levels fell to 1.7±0.3 mmol l1 and remained stable thereafter.
|
During prolonged exercise of moderate intensity, glucose 6-phosphate remained stable at pre-exercise levels in all muscles (Fig. 3). However, in response to the subsequent intense sprint, glucose 6-phosphate increased above resting levels in all muscles, with the exception of the white gastrocnemius muscle. During recovery, glucose 6-phosphate in all muscles returned to rest levels within 30 min, and remained at low and stable levels thereafter (Fig. 3).
|
Effects of a combination of moderate and high intensity exercise on the fractional velocity of glycogen synthase during and after exercise
In response to exercise of moderate intensity, the fractional velocities of
glycogen synthase increased above rest levels in the mixed, white and red
gastrocnemius and the mixed quadriceps muscles
(Fig. 4). At the onset of
recovery from the subsequent sprint, the fractional velocities of glycogen
synthase did not increase further in any of the muscles
(Fig. 4). During recovery, the
fractional velocities of glycogen synthase remained above basal level in the
mixed and white gastrocnemius muscles (Fig.
4). In the red gastrocnemius and mixed quadriceps muscles, the
fractional velocities of glycogen synthase returned to basal pre-exercise
levels within 60 min of recovery and remained stable throughout the remaining
of the recovery period (Fig.
4).
|
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Discussion |
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Since, in fasted rats, the extent of muscle glycogen repletion following an intense sprint effort is not limited by the amount of accumulated lactate, this raises the issue of the identity and relative contributions of the different carbon sources recruited for glycogen synthesis. During the first 30 min of recovery, a role for lactate is suggested by the fall in plasma and muscle lactate levels coinciding with glycogen synthesis (Figs 1, 2). However, since during the later stages of recovery (30120 min), glycogen increases further in all of the muscles examined, despite the absence of any change in muscle and plasma lactate levels (Figs 1, 2), this suggests that the synthesis of muscle glycogen during that stage involves net carbon sources other than lactate, such as glycerol and amino acids derived from triglyceride hydrolysis and protein breakdown, respectively. Hepatic glycogen stores, however, are unlikely to play any role in this process given that they remain at stable levels throughout recovery.
Across the different muscles examined in this study, the carbon sources other than lactate (e.g. amino acids, glycerol) are likely to have contributed at the very least 43, 65, 36 and 49% of the total amount of muscle glycogen replenished during the whole recovery period in the mixed, white, and red gastrocnemius and quadriceps muscles, respectively, with the remainder carbon source being lactate. These are highly conservative estimates calculated simply by determining the proportion of glycogen deposited during the 30120 minrecovery period when there is no change in plasma and muscle lactate levels, relative to the total increase in glycogen levels over the whole duration of the recovery period. The underlying assumption on which these calculations are based are that all the glycogen synthesised while lactate levels are falling during early recovery occurs exclusively at the expense of the pool of accumulated lactate, either directly or indirectly via lactate conversion to glucose. This assumption is most probably unrealistic, since carbon sources other than lactate (glycolytic intermediates, glycerol, amino acids) might contribute to glycogen synthesis during the first 30 min of recovery. For instance, the fall in glucose 6-phosphate levels during that time could have contributed to the synthesis of glycogen (Fig. 1). For these reasons, the actual contributions of carbon sources other than lactate to the synthesis of glycogen are likely to be much higher, and that of lactate much lower, than those calculated here. Although the exact relative contributions of all carbon sources remain to be established, our findings show that lactate availability does not impose an upper limit on the levels of glycogen attained during recovery from high intensity exercise.
Our findings are consistent with the view that skeletal muscles possess
critical levels of glycogen that are protected against sustained depletion,
and that the extent of muscle glycogen repletion during recovery from an
intense effort in fasted animal is determined primarily by the amount of
glycogen required to attain those protected levels, irrespective of lactate
availability (Raja et al.,
2003). This is supported by our observations that the levels of
muscle glycogen attained during recovery from a combination of moderate and
high intensity exercise (Fig.
1) are comparable to those attained during recovery from a wide
range of different protocols of high intensity exercise in fasted rats, such
as a single sprint or multiple short sprints
(Ferreira et al., 2001
;
Raja et al., 2003
).
It is noteworthy that the levels at which the stores of muscle glycogen are
protected against sustained depletion in fasted rats are high enough to
support a little more than one bout of an intense sprint effort to exhaustion.
Similarly, following high intensity exercise, most animal species in the
fasted state (e.g. fish, amphibians, snakes, lizards and humans) also
replenish their muscle glycogen stores to levels such that they can engage in
at least one bout of intense sprint to exhaustion without being limited by the
size of their glycogen stores (Hermansen
and Vaage, 1977; Gratz and
Hutchison, 1977
; Gleeson,
1982
; Astrand et al.,
1986
; Milligan and Wood,
1986
; Peters-Futre,
1987
; Gleeson,
1989
; Scarabello et al.,
1992
; Fournier and Guderley,
1992
; Girard and Milligan, 1993;
Choi et al., 1994
;
Milligan, 1996
;
Bangsbo et al., 1997
). Such a
capacity is important because there are extreme circumstances associated with
`flight or fight' behaviour where an animal might have to engage in a sprint
to near exhaustion (Raja et al.,
2003
). Had accumulated lactate been the major determinant of
glycogen accumulation in the present study, the levels of muscle glycogen
attained post-exercise would have been not only much lower than those reported
here, but also probably low enough to impair the capacity of skeletal muscle
to engage in subsequent unimpaired fight or flight responses.
The dephosphorylation-mediated activation of glycogen synthase is likely to
play some role in enabling muscles to increase their glycogen to levels well
in excess of those that would be attained if lactate were limiting glycogen
accumulation. Consistent with this view, glycogen synthase in the red
gastrocnemius and mixed quadriceps muscles is activated at the onset of
recovery while net glycogen synthesis is taking place, but returns to
pre-exercise basal activation state when glycogen reaches stable levels (Figs
1,
4). Moreover, the progressive
increase in the glycogen content of the mixed and white gastrocnemius muscles
throughout the 120 min recovery period is associated with the maintenance of
higher than basal fractional velocities of glycogen synthase during that time
(Figs 1,
4). It remains to be shown,
however, whether an eventual return of the fractional velocity of glycogen
synthase to basal levels in these muscles would also coincide with muscle
glycogen returning to stable levels as observed for the mixed quadriceps and
white gastrocnemius muscles. That this might be the case is suggested from the
observation that, during recovery from a sprint performed by previously rested
rats, the fractional velocity of glycogen synthase is at its highest at the
onset of recovery when glycogen repletion is taking place, and returns to
basal levels within only 30 min of recovery in the mixed, white and red
gastrocnemius muscles at a time when the stores of muscle glycogen reach
stable levels (Ferreira et al.,
2001).
Given that there are physiological conditions where both the
phosphorylation state and activation state of glycogen synthase are controlled
by glucose 6-phosphate levels (Bloch et
al., 1994), the question arises of whether a higher than basal
level of glucose 6-phosphate contributes to the sustained activation of
glycogen synthase and glycogen synthesis during recovery from a combination of
moderate and high intensity activity. The elevated levels of glucose
6-phosphate at the onset of recovery in this study might contribute to the
initial activation of glycogen synthesis, but the early return of this
metabolite to basal pre-exercise levels, despite ongoing glycogen synthesis
until late into recovery, suggests that glucose 6-phosphate does not play a
major role in the control of glycogen synthesis during late recovery
(Fig. 3). This constitutes one
of several physiological conditions where changes in glucose 6-phosphate
levels do not play a major role in the control of the rate of glycogen
synthesis in skeletal muscles (James et
al., 1998
; Lawrence and Roach, 2000;
Fournier et al., 2002
).
In conclusion, this study shows that the availability of accumulated lactate is not the major factor limiting glycogen repletion during recovery from an intense sprint effort in fasted rats. Instead, our findings support the view that skeletal muscles possess set levels of glycogen that are protected against sustained depletion, and that the amount of glycogen required to attain these levels determines the extent of glycogen synthesis during recovery from a sprint, irrespective of lactate availability. The sustained dephosphorylation-mediated activation of glycogen synthase, but not glucose 6-phosphate, might play an important role in this process. More research, however, is required to elucidate the nature of the mechanisms that set the levels at which muscle glycogen is protected against sustained depletion and whether these set levels can be altered. Finally, it remains to be established whether it is generally the case across animal species that the amount of accumulated lactate does not limit the level of muscle glycogen attained during recovery from a short sprint effort. The experimental design adopted here might prove helpful in addressing some of these questions.
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Acknowledgments |
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