Repeated bouts of high-intensity exercise and muscle glycogen sparing in the rat
1 School of Human Movement and Exercise Science, The University of Western
Australia, Crawley, Western Australia 6009, Australia
2 Department of Molecular Biology, James Cook University, Townsville,
Queensland 4811, Australia
* Author for correspondence (e-mail: fournier{at}cyllene.uwa.edu.au)
Accepted 28 March 2003
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Summary |
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Key words: exercise, fasting, glycogen, lactate, skeletal muscle, recovery, rat
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Introduction |
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Fortunately, even in the absence of food intake, muscles recovering from
physical activity have the capacity to replenish some or even all of their
glycogen stores (reviewed in Fournier et
al., 2002). In particular, during recovery from a maximal sprint
effort, muscles replenish at least part of their glycogen stores. Under these
conditions, lactate is the most likely carbon source for glycogen synthesis,
either directly or indirectly via its conversion to glucose
(Gleeson, 1996
;
Palmer and Fournier, 1997
;
Fournier et al., 2002
). This
synthesis of muscle glycogen from endogenous carbon sources has been
demonstrated not only in humans and rats
(Fournier et al., 2002
) but
also in a variety of other animals including fish
(Milligan and Wood, 1986
;
Pagnotta and Milligan, 1991
;
Girard and Milligan, 1992
;
Scarabello et al., 1992
;
Milligan, 1996
), amphibians
(Fournier and Guderley, 1992
),
snakes (Gratz and Hutchison,
1977
) and lizards (Gleeson,
1982
,
1996
;
Gleeson and Dalessio,
1989
).
Although it is generally the case that animals recovering from
high-intensity physical activity can replenish their muscle glycogen stores in
the absence of food intake, it is important to note that most lower
vertebrates (Gratz and Hutchison,
1977; Gleeson,
1982
,
1996
;
Milligan and Wood, 1986
;
Gleeson and Dalessio, 1989
;
Pagnotta and Milligan, 1991
;
Fournier and Guderley, 1992
;
Girard and Milligan, 1992
;
Scarabello et al., 1992
;
Milligan, 1996
) and some
mammal species (Bräu et al.,
1999
) have the capacity to replenish their muscle glycogen stores
completely under these conditions whereas the replenishment of muscle glycogen
is only partial in other species of mammals, such as humans and rats
(Hermansen and Vaage, 1977
;
Astrand et al., 1986
; Bangsbo
et al., 1992
,
1997
;
Choi et al., 1994
;
Nikolovski et al., 1996
;
Peters et al., 1996
;
Ferreira et al., 2001
). On
this basis, one might propose that in those animals where the extent of
glycogen repletion is only partial post-exercise, a few consecutive bouts of
high-intensity physical activity might eventually lead to a progressive
decrease in the levels of muscle glycogen attained after each consecutive
recovery period. Unless mechanisms exist to protect muscle glycogen against
sustained depletion, muscle glycogen would be expected to eventually attain
levels low enough to impair the ability of these animals to engage in
fight-or-flight behaviours (Balsom et al.,
1999
). Since the rat is one animal species where glycogen
repletion post intense exercise is only partial without food intake, the aim
of this study was to assess whether, as predicted, repeated consecutive bouts
of high-intensity exercise in the rat will eventually result in the sustained
depletion of their stores of muscle glycogen or whether mechanisms exist for
the sparing of their muscle glycogen stores.
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Materials and methods |
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Animals
Adult male albino Wistar rats (Rattus norvegicus Berkenhout;
280320 g) were obtained from the Animal Resource Centre at the
University of Murdoch, 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 light:dark
photoperiod and had unlimited access to water and a standard laboratory chow
diet (Glen Forrest Stockfeeders, Glen Forrest, Western Australia: 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) so as to prevent hepatic glycogen and food present
in the gut from providing carbon precursors for the replenishment of muscle
glycogen post-exercise. All experiments took place between 8.00 h and 13.00 h.
This research project was approved by the Animal Ethics Committee of the
University of Western Australia.
Exercise protocol
As rats are natural swimmers, an exercise protocol based on swimming was
adopted for this study, the intensity of the exercise being similar for each
exercise bout and determined by the amount of lead weight attached to the base
of the tail (Ferreira et al.,
2001). The advantage of this exercise protocol over one that uses
a treadmill is that a prolonged training period is not required for rats to
exercise at near-maximal intensity and this protocol results in reproducible
glycogen mobilisation and lactate accumulation
(Nikolovski et al., 1996
;
Ferreira et al., 2001
).
Immediately before swimming, each rat was weighed and a lead weight equivalent
to 10% body mass was attached to the base of its tail. Each rat swam for 3 min
in a plastic tank (30 cm diameter, 48 cm depth) filled with water at 34°C
as described previously (Ferreira et al.,
2001
). With the exception of one group of non-exercised rats,
which served as the control group, all animals were subjected to either one,
two or three bouts of exercise, each bout being separated from the next one by
a recovery period of 60 min. The animals were sacrificed either immediately
following each bout of exercise or after each of the associated 60 min
recovery periods during which each rat recovered alone in a cage without
access to food. Other animals were subjected to only one bout of
high-intensity exercise and were allowed to recover individually in separated
cages for either 0, 10, 20, 40, 60 or 120 min prior to being sacrificed.
Tissue sampling
The study examined different muscles selected on the basis of their fibre
compositions. The white, red and mixed gastrocnemius muscles were selected
because they are actively recruited during high-intensity swimming and are
rich in fast-twitch white, fast-twitch red and a combination of both fibre
types, respectively, but are poor in slow-twitch red fibres, thus reflecting
the composition of the hindlimb musculature as a whole
(Maltin et al., 1989). By
contrast, the soleus muscle, which is rich in slow-twitch red fibre, was
chosen on the basis that its glycogen stores are not recruited during
high-intensity swimming (Nikolovski et
al., 1996
; Ferreira et al.,
2001
).
Rats at rest or at time intervals during the post-exercise recovery period
were anaesthetised under halothane as described previously
(Ferreira et al., 1998), and
their tissues, namely individual muscles (soleus muscle and red, white and
mixed gastrocnemius muscles), blood and liver, were sampled. After removal,
each 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 and processed as
described below.
Extraction of blood and tissue metabolites
Immediately following its removal from the heart, blood was transferred
into a heparinised Eppendorf microcentrifuge tube and centrifuged immediately
at 720 g for 5 min. Following 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, while the remaining plasma
was stored at -80°C. After centrifugation, the supernatant was neutralised
with 2 mol l-1 K2CO3 and centrifuged at 2000
g for 10 min. All samples were kept at -80°C until
analysed.
Muscles were weighed and ground under liquid nitrogen
(Lehoux and Fournier, 1999),
and the powdered tissue was homogenised with 10 volumes of ice-cold 6%
perchloric acid. A portion of the homogenate was used for the determination of
glycogen, while a 700 µl aliquot was centrifuged at 2000 g
for 10 min and the supernatant removed and kept on ice. The pellet was
re-extracted with 350 µl of 6% perchloric acid before re-centrifugation at
2000 g for 10 min. Following centrifugation, the two
supernatants were combined, neutralised with 2 mol l-1
K2CO3 and centrifuged before being stored at -80°C
until analysis of metabolites. The levels of glycogen, lactate, glucose,
glucose 6-phosphate, glycerol, ß-hydroxybutyrate and acetoacetate were
assayed as described by Bergmeyer
(1974
), and fatty acid levels
were determined using the Wako NEFA C Kit (Wako Pure Chemicals Industries,
Osaka, Japan).
Expression of results and statistical analyses
All metabolite concentrations in tissues and plasma are expressed in
µmol g-1 wet mass and mmol l-1, respectively, and
results are expressed as means ± S.E.M.
(N=812). The effects of exercise and post-exercise recovery on
the levels of metabolites in muscles and plasma were analysed with a
one-factor analysis of variance (ANOVA) followed by a Fisher protected least
significant difference a posteriori test using Stat View SE +
Graphics version 1.03 (Abacus Concepts, Berkeley, CA, USA).
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Results |
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|
Effect of repeated bouts of high-intensity exercise and recovery on
lactate levels in muscle
Repeated bouts of high-intensity exercise, each separated by a 1 h recovery
period, resulted in a significant increase in muscle lactate levels
(Fig. 2). The extent of lactate
accumulation in the soleus muscle and red, white and mixed gastrocnemius
muscles was highest in response to the first bout of exercise. During the
recovery period following each bout of exercise, lactate levels returned to
pre-exercise levels in all muscles examined.
|
Effect of repeated bouts of high-intensity exercise on plasma
metabolite levels
Each bout of high-intensity exercise resulted in a significant increase in
the levels of plasma lactate (Fig.
3). By contrast, the levels of plasma glucose
(Fig. 3) and glycerol
(Fig. 4) were not significantly
affected by the first bout of exercise, but glucose levels decreased in
response to both the second and third exercise bouts
(Fig. 3). With respect to the
levels of plasma fatty acids, acetoacetate and ß-hydroxybutyrate, a
distinct pattern of changes took place in response to each bout of exercise
and ensuing recovery period. Each bout of exercise resulted in a significant
decrease in the levels of plasma fatty acids, acetoacetate and
ß-hydroxybutyrate (Fig.
4). During each of the recovery periods, these metabolites
returned to levels comparable or higher than those before exercise, with their
concentrations after the third exercise bout being higher than basal
pre-exercise levels. In particular, the levels of ß-hydroxybutyrate
reached after each period of recovery showed a gradual increase to levels
that, after the third recovery period, were well above those after the first
recovery period (Fig. 4).
|
|
In response to a single bout of exercise, glycerol remained at stable levels, whereas the levels of plasma free fatty acids, acetoacetate and ß-hydroxybutyrate decreased significantly (Fig. 5). During recovery, the levels of glycerol remained unchanged while those of fatty acids, acetoacetate and ß-hydroxybutyrate increased progressively (Fig. 5).
|
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Discussion |
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On the basis of our findings, one must amend the view that rats recovering
from high-intensity exercise differ from most species of lower vertebrates in
that, in the absence of food intake, they are incapable of replenishing
completely their glycogen stores. Here, we show that there are conditions
where the glycogen mobilised in response to a sprint is completely replenished
after exercise in fasted rats (Fig.
1). Furthermore, the observation that repeated sprints fail to
cause a progressive fall in the levels of muscle glycogen attained after each
consecutive recovery period might be taken as evidence that there is a
critical amount of muscle glycogen in the rat that is protected against
sustained depletion. In order to support further this interpretation, other
studies would be required to show that glycogen levels post-exercise are
protected irrespective of the type, intensity and duration of exercise and
availability of endogenous carbon sources. Fortunately, one such study has
been performed in which fasted Wistar rats were forced to engage for nearly
2.5 h in continuous or intermittent aerobic exercise in order to deplete
aerobically most of their muscle glycogen stores
(Gaesser and Brooks, 1980).
This study reported that during recovery, the stores of muscle glycogen
increased to levels (17.6 µmol g-1) comparable with those
observed in the present study in response to either one or several 3-min
sprints, but with the difference that endogenous carbon sources other than
lactate were involved since these aerobic exercise protocols resulted only in
a marginal increase in blood lactate level
(Gaesser and Brooks, 1980
).
Overall, the observations that in fasted rats muscle glycogen levels return to
comparable levels in response to a range of highly different exercise
protocols, such as a single 3-min sprint, multiple 3-min sprints, prolonged
continuous aerobic exercise or prolonged intermittent aerobic exercise,
provide strong support for the existence in skeletal muscles of set glycogen
levels that are protected against sustained depletion post-exercise.
It is interesting to note that the levels at which muscle glycogen levels
are protected against sustained depletion in the rat are high enough to
support a little more than one bout of an intense sprint effort to exhaustion.
Normally, during a sprint to exhaustion, it is the accumulation of
H+ and inorganic phosphate ions rather than the depletion of muscle
glycogen that causes fatigue (Fitts and
Metzger, 1993). However, if muscle glycogen stores were to be
protected at much lower levels, the limited supply of glycogen would become
the main factor limiting an animal's capacity to engage in an intense sprint
to exhaustion by causing premature fatigue
(Balsom et al., 1999
).
Although, under most conditions, a sprint would be expected to last only a few
seconds, there are extreme conditions associated with fight-or-flight
behaviour where an animal might have to engage in a sprint to near exhaustion.
For these animals, it would be highly advantageous to maintain their muscle
glycogen stores at levels high enough so that the build-up of H+
and inorganic phosphate ions, rather than the size of their glycogen stores,
limits their capacity to engage in an intense sprint effort to exhaustion. In
this regard, it is noteworthy that after a sprint most animal species in the
fasted state generally 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
;
Gleeson and Dalessio, 1989
;
Astrand et al., 1986
;
Milligan and Wood, 1986
;
Scarabello et al., 1992
;
Fournier and Guderley, 1993; Girard and
Milligan, 1992
; Choi et al.,
1994
; Milligan
1996
; Bangsbo et al.,
1997
).
In light of the above discussion, the observation that glycogen repletion
in the rat is only partial after a single bout of exercise
(Fig. 1) may be explained on
the basis that muscle glycogen levels in 24 h-fasted rats are higher than the
minimal critical levels normally protected in this species. Along this line of
reasoning, the observation that in several vertebrate species the stores of
muscle glycogen are completely replenished after a single bout of intense
exercise (Gratz and Hutchison,
1977; Gleeson,
1982
,
1996
;
Milligan and Wood, 1986
;
Gleeson and Dalessio, 1989
;
Pagnotta and Milligan, 1991
;
Fournier and Guderley, 1992
;
Girard and Milligan, 1992
;
Scarabello et al., 1992
;
Milligan, 1996
;
Bräu et al., 1999
) might
be explained on the basis that their muscle glycogen stores are kept at their
species-specific protected levels. This raises the novel question of whether
the muscle glycogen stores in these animal species would also be only
partially replenished post high-intensity exercise if one were to manipulate
their glycogen stores so that more than protected glycogen levels were to be
stored in their muscles prior to exercise. This is an issue that remains to be
investigated.
The capacity of fasted rats to replenish their muscle glycogen stores
between each consecutive bout of exercise raises the question of the identity
of the carbon sources mobilised for the synthesis of glycogen. Since, in the
present study, the animals were in a fasted state, the synthesis of muscle
glycogen had to depend solely on endogenous substrates. The lactate built up
in response to exercise is a likely candidate
(Fig. 3), as it is generally
acknowledged as one of the major carbon sources for the synthesis of muscle
glycogen in many vertebrate species
(Gleeson, 1996;
Palmer and Fournier, 1997
;
Fournier et al., 2002
). That
lactate is also likely to be a major carbon source for the replenishment of
muscle glycogen during recovery from each bout of exercise in rats is
suggested indirectly by the observation that the fall in plasma and muscle
lactate levels is temporally linked with glycogen synthesis. In this respect,
the changes in lactate levels in the soleus muscles may seem at first
surprising, considering the absence of net glycogen breakdown and synthesis in
this muscle, but, as argued before
(Bräu et al., 1997
;
Ferreira et al., 2001
), it is
more than likely that the exercise-mediated rise and subsequent fall in
lactate levels in this muscle result from an exchange of lactate between the
soleus muscle and the blood. The stores of hepatic glycogen are unlikely to
provide a net source of glucose for the resynthesis of muscle glycogen stores,
since liver glycogen remains at stable levels in response to several sprints
and recovery periods. It is important to stress that amino acids and glycerol
via their conversion to glucose by the liver could contribute to the
replenishment of muscle glycogen (Gaesser
and Brooks, 1980
; Fournier et
al., 2002
), but their relative contributions, as well as that of
lactate, remain to be established.
The mechanisms by which the proportion of muscle glycogen replenished
post-exercise differs between the first and subsequent bouts of exercise
remain to be elucidated. Any attempt at explaining this finding must take into
consideration the observation that the absolute amount of glycogen deposited
during recovery from the first exercise bout is not different from that after
each subsequent bout (Fig. 1). It is because more glycogen is mobilised during the first exercise bout than
during the following bouts, maybe because of a higher work output, that the
proportion of muscle glycogen replenished after the first exercise bout is
lower than after the other two exercise bouts. It is interesting to note that
such a lower extent of glycogen mobilisation and lactate accumulation in
response to the second and third bouts of high-intensity exercise is not
shared by all animals species, since, in the rainbow trout (Oncorhynchus
mykiss), for instance, the extent of glycogen mobilisation and lactate
accumulation does not differ between consecutive exercise bouts
(Scarabello et al., 1992).
Considering that in the rat more lactate is eliminated during recovery from
the first exercise bout than during subsequent bouts (Figs
2,
3), with equivalent amounts of
muscle glycogen being replenished, a lower proportion of lactate is likely to
be converted into glycogen during recovery from the first bout of exercise.
This interpretation holds as long as lactate is the main carbon source for
glycogen synthesis, and this might partly explain the partial replenishment of
muscle glycogen stores in response to a single bout of exercise.
The differences in the pattern of glycogen repletion between the first and
subsequent bouts of exercise raise the question of whether other aspects of
fuel metabolism differ among these bouts of exercise. We have addressed this
question indirectly by examining the effects of a single bout as well as that
of repeated bouts of high-intensity exercise on plasma levels of glycerol,
free fatty acids, ß-hydroxybutyrate and acetoacetate. As reported
previously by others in humans and rats
(Drury et al., 1941;
Balasse et al., 1978
;
Romijn et al., 1993
), the
levels of plasma fatty acids and ketone bodies decreased significantly from
rest levels in response to a single bout of high-intensity exercise and
increased throughout recovery to attain levels comparable with or higher than
those measured before exercise (Figs
4,
5). The impact of repeated
bouts of high-intensity exercise on the plasma levels of fatty acids,
acetoacetate and ß-hydroxybutyrate suggests that the metabolic state of
the rat prior to the second and third bouts of exercise was different from
that before the first bout (Fig.
4). Indeed, the levels of plasma fatty acids and ketone bodies
attained after each of the recovery periods were higher than those prior to
the first exercise bout (Fig.
4). Since the rates of utilisation of fatty acids and ketone
bodies by muscle are partly determined by their concentrations
(Newsholme and Leech, 1983
),
the higher levels of fatty acids and ketone bodies prior to the second and
third bouts of high-intensity exercise, as well as during recovery from these
bouts, would be expected to enhance their oxidation by muscles. As a result,
this would be predicted to provide muscles and other organs with an increased
supply of fuels other than glucose and lactate to support their energy
demands, particularly during recovery from exercise. Assuming lactate is the
major carbon source for glycogen synthesis, this lesser oxidation of lactate
and of glucose derived from lactate might allow for an increased proportion of
lactate converted into muscle glycogen after the second and third bouts of
exercise. This might also explain the higher proportion of glycogen
replenished during recovery from these exercise bouts. Irrespective of whether
this explanation holds, our findings clearly suggest that several aspects of
fuel metabolism differ between the first and subsequent bouts of exercise and
that this must be taken into consideration when attempting to explain the
increased sparing of muscle glycogen in response to several bouts of exercise.
It is not clear, however, the extent to which these differences might partly
result from possible differences in work output between the first and
subsequent exercise bouts. Moreover, different hormonal responses might also
exist between the first and subsequent exercise bouts and explain also, at
least in part, the differences in the pattern of glycogen metabolism between
consecutive sprints.
In conclusion, our results corroborate earlier findings that glycogen repletion is only partial in fasted rats recovering from a single bout of high-intensity exercise. However, this study indicates that mechanisms exist to ensure that muscles from fasted rats can replenish completely their stores of glycogen if subjected to more than one bout of high-intensity exercise. Rats, therefore, resemble many other vertebrate species in that without food intake they can also protect their muscle glycogen against sustained depletion by replenishing completely their glycogen stores post-exercise to support the energy demands associated with fight-or-flight behaviour. Since, following high-intensity exercise, muscle glycogen repletion from endogenous carbon sources is only partial in other mammal species, such as humans, it remains to be established whether our findings in the rat are typical of mammals in general.
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Acknowledgments |
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