A regulatory role for cortisol in muscle glycogen metabolism in rainbow trout Oncorhynchus mykiss Walbaum
Department of Biology, The University of Western Ontario, London, ON N6A 5B7 Canada
e-mail: milligan{at}uwo.ca
Accepted 10 June 2003
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Summary |
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Key words: rainbow trout, Oncorhynchus mykiss, cortisol, muscle, glycogen, exercise, glycogen phosphorylase, glycogen synthase, metapyrone
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Introduction |
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The rate at which muscle glycogen is synthesized is a function of the
relative activities of glycogen synthase (GSase) and glycogen phosphorylase
(Phos). The activity of these enzymes is regulated by a complex
phosphorylation/dephosphorylation cycle. Both Phos and GSase exist in two
interconvertible forms, active and inactive (nominally). Phosphorylation of
glycogen phosphorylase (converting Phos b to Phos a), leads
to an increase in activity, whereas phosphorylation of glycogen synthase
(converting GSase I to GSase D) decreases its activity (e.g.
Connett and Sahlin, 1996).
These transformations are regulated hormonally (by, for example, adrenaline,
glucagon) via cAMP-mediated activation of kinases and
contraction-induced changes in intracellular Ca2+ (for a review,
see Connett and Sahlin, 1996
).
Glucocorticoids have also been implicated in regulating these enzymes, at
least in liver (see Mommsen et al.,
1999
). However, little evidence exists to suggest a similar
regulatory role for glucocorticoids in muscle. In addition, both Phos
a and GSase I activities are influenced by substrate
availability (Pi and glucose-6-phosphate, respectively) and changes
in allosteric modifiers (e.g. AMP and ADP; Shulman et al., 1995;
Shulman and Rothman, 1996
;
Howlett et al., 1998
).
Relative levels of Phos a are likely to be the dominant factor
controlling glycogenolysis because this enzyme not only catalyzes the initial
rate-limiting step in glycogenolysis, but also inhibits glycogenesis by
blocking conversion of GSase D to GSase I
(Connett and Sahlin, 1996
).
The rate-limiting step to glycogen synthesis, at least in mammalian muscle,
appears to be shared between glucose transport and glycogen synthase activity,
depending upon the nutritional state of the organism
(Shulman and Rothman, 1996;
Howlett et al., 1998
;
Fisher et al., 2002
). The story
is likely to be somewhat different in fish muscle because of the relatively
low rates of glucose uptake in the latter
(West et al., 1993
) and the
minor contribution made by blood glucose to muscle glycogen synthesis
(Pagnotta and Milligan, 1991
).
Although glucose transporters have been identified in fish muscle
(Legate et al., 2001
;
Teerijoki et al., 2001
), their
physiological role is unclear. As has been described for mammalian muscle
(Montell et al., 1999
),
glycogen levels themselves may dictate the activity of GSase and subsequently,
the rate of net glycogen synthesis (e.g.
Parkhouse et al., 1988
).
The purpose of this study was therefore to investigate the role of cortisol
in regulating muscle glycogen synthesis. Changes in white muscle glycogen
synthase and phosphorylase activities in rainbow trout during recovery from
exhaustive exercise were followed in fish that had been treated prior to
exercise with metyrapone to block cortisol synthesis (see
Eros and Milligan, 1996). To
confirm that the effects seen were cortisol-specific, metyrapone-treated fish
were infused with cortisol after exercise, in an attempt to mimic the
post-exercise rise in cortisol seen in the control fish.
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Materials and methods |
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Fish were surgically fitted with a dorsal aorta cannula
(Soivio et al., 1972) while
under MS-222 anesthesia (1:10,000 dilution, adjusted to pH 7.0 with
NaHCO3). Fish were allowed to recover for at least 48 h in black
acrylic fish boxes continuously supplied with aerated, dechlorinated tapwater
at the experimental temperature. During this period fish were not fed. The
catheters were checked daily and filled with heparinized (50 i.u.
ml1 sodium-heparin, Sigma) saline.
Experimental protocol
Fish were randomly assigned to one of three experimental groups: saline
injected (control, N=8), metyrapone + saline injected (metyrapone
group, N=8) or metyrapone + cortisol injected (cortisol group,
N=8). 1 h prior to exercise, fish were injected with either 3 mg 100
g1 metyrapone (2-methyl-1, 2-di-3-pyridyl-1-propanone; Sigma
Chemical, St Louis, MO, USA) or an equivalent volume, 20 µl 100
g1, of 0.9% NaCl. Fish were then transferred to a large
circular tank (300 liter) and manually chased around the tank for 5 min, at
which point they were unresponsive to further stimuli and considered
exhausted. This method of exhausting fish has been used extensively and
results in consistent metabolic disturbances (for a review, see
Milligan, 1996). Fish were
returned to their individual boxes, where they were able to freely move about,
until sampled.
Half of the metyrapone-treated fish were injected with either 30 µg 100 g1 cortisol (hemisuccinate cortisol, Sigma; cortisol group) and the other half received an equivalent volume (20 µl 100 g1) of 0.9% NaCl (metyrapone group). The control fish were injected with 20 µl 100 g1 0.9% NaCl.
Individual fish were sampled only once, either 1 h after metyrapone or saline injection (termed `rest'), immediately after exercise to exhaustion (time 0) or at 1, 2 or 4 h post-exercise. Fish sampled at time 0 had only been injected with either saline or metyrapone. Cortisol injection was administered after exercise, so the cortisol group was not sampled until 1 h post-exercise. At the appointed time after exercise, 500 µl of blood was withdrawn from the catheter into a gas-tight Hamilton syringe and placed on ice until analyzed. The fish was then killed by anaesthetic overdose (2.0 g l1 buffered MS-222) and a sample of white muscle was excised from the dorsal-epaxial muscle mass. The muscle sample was freeze-clamped between aluminum plates pre-cooled with liquid N2 and stored at 80°C prior to analysis. A 50 µl sample of whole blood was added to 200 µl of ice-cold 8% HClO3, mixed, then centrifuged at 10 000 g for 5 min. The supernatant was withdrawn and stored at 4°C until analysis for lactate. The remaining blood was centrifuged at 10 000 g for 5 min, and the plasma stored at 80°C for analysis of cortisol and catecholamines.
Analytical techniques and calculations
Whole blood lactate was measured enzymatically on 100 µl of the
deproteinized HClO3 extract using Sigma lactate reagents and
procedures described by Bergmeyer
(1965). Cortisol was measured
on 25 µl duplicate samples of plasma using a commercially available
radio-immunoassay kit (ICN Biomedicals, Costa Mesa, CA, USA). The lower limit
of detection of this assay was 1.5 ng ml1 and the intra- and
inter-assay coefficients of variation were 7.3 and 8.5%, respectively. Plasma
adrenaline and noradrenaline levels were measured on alumina-extracted samples
using high pressure liquid chromatography (Beckman System Gold, Fullerton, CA,
USA) with electrochemical detection (ESA Coulochem II, Chelmsford, MA, USA),
according to the method of Woodward
(1982
). Dihydroxybenzylamine
hydrobromide (DHBA) was used as an internal standard in all samples.
For measurement of muscle lactate, glucose and glucose-6-phosphate, muscle
was ground to a fine powder in a liquid N2-cooled mortar.
Approximately 100 mg of powdered tissue were added to 1.0 ml of ice-cold 8%
HClO3 and vigorously mixed with a vortex mixer for 1 min.
Homogenates were centrifuged for 5 min at 10 000 g and the
supernatant withdrawn and stored at 4°C for up to 1 week until analyzed
for lactate concentration, as described above for blood. Muscle glycogen was
measured on approximately 100 mg of frozen muscle, which was placed directly
into 1.0 ml of 30% KOH and digested in a boiling water bath. Glycogen was
isolated as described by Hassid and Abraham
(1957) and measured as free
glucose following digestion with amyloglucosidase
(Bergmeyer, 1965
).
Glycogen phosphorylase (Phos, EC 2.4.1.1) was measured on muscle ground to
a fine powder under liquid nitrogen in a liquid nitrogen-cooled mortar as
described by Storey (1991). In
brief,
150 mg of powdered, frozen tissue was transferred to a test tube
containing 1 ml ice-cold homogenization buffer (50 mmol l1
imidazole, 100 mmol l1 NaF, 5 mmol l1
EGTA, 2 mmol l1 EDTA, 30 mmol l1
2-mercaptoethanol, 0.1 mmol l1 phenylmethylsulfonylflouride)
and homogenized on ice for 3x 10 s bursts with a Tissue Tearor (Biospec
Products, Bartlesville, OK, USA) set to speed 6. The samples were allowed to
settle on ice for 15 min and the supernatant was assayed for enzyme activity.
Phos a activity was measured in 50 mmol l1
potassium-phosphate buffer (pH 7.0) containing 2 mg ml1
glycogen (oyster muscle, dialyzed), 0.4 mmol l1 NAD, 10
µmol l1 glucose-1,6-bisphosphate, 0.25 mmol
l1 EDTA, 150 mmol l1 MgCl2 and
1.4 U ml1 phosphoglucomutase and 0.5 U ml1
glucose-6-phosphate dehydrogenase. Total Phos (a+b) activity
was measured in the presence of 1.6 mmol l1 5'AMP.
Absorbance changes were measured at 340 nm on a UV-160 recording
spectrophotometer (Shimadzu, Columbia, MD, USA). All enzyme activities were
measured at 15°C. Enzyme activities are expressed per unit wet mass.
Glycogen synthase (GSase; EC 2.4.1.11) was measured on100 mg of
powdered muscle mixed vigorously for 2 min on a vortex mixer at maximum speed,
with 1 ml homogenization buffer (50 mmol l1 Tris, 0.5 mmol
l1 dithiothrietol, 1.0 mmol l1 EDTA, 2.0
mmol l1 MgCl2, pH 7.8
(Schallin-Jantti et al.,
1992
). GSase activity measured in samples processed this way were
less variable and more consistent with previously published values, compared
to values obtained from tissues processed using a mechanical tissue
homogenizer. The sample was briefly centrifuged (1 min at 10 000
g), and the supernatant assayed for glycogen synthase
activity. Glycogen synthase activity in the supernatant was measured in the
presence (I + D forms) or absence (I active form only) of 5
mmol l1 glucose-6-phosphate. Glycogen synthase activity is
expressed as the ratio of I:I+D. The assay mixture contained
70 mmol l1 KCl, 50 mmol l1 Tris, 7 mmol
l1 MgCl2, 5 mmol l1
phosphoenolpyruvate, 0.15 mmol l1 NADH, 2.5 U 10
ml1 lactate dehydrogenase, 5 U 10 ml1
pyruvate kinase and 20 mmol l1 UDP-glucose. A blank from
each homogenate, which did not contain UDP-glucose, was assayed simultaneously
and subtracted from all GSase measurements. The change in absorbance over time
at 340 nm was monitored at 15°C, as described above.
All biochemicals were purchased from Sigma Chemical Co. (St Louis, MO, USA) or Boehringer-Mannheim (Lachine, Quebec, Canada); all other reagents were acquired from local suppliers and were of the highest available purity.
Statistical analysis
All values are presented as means ± 1 S.E.M. Significant
differences within a group were assessed with a one-way analysis of variance
(ANOVA) and, where appropriate, followed by a Dunnett's analysis to compare
within-group times to the respective pre-exercise value. Significant
differences between groups at a given time were assessed using Student's
t-test, unpaired design. Differences were considered significant if
P<0.05.
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Results |
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Concentrations of circulating catecholamines were significantly elevated post-exercise in all groups (Fig. 2A,B) and had declined to levels not different from pre-exercise rest values by 1 h post-exercise.
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In all groups, the exercise regime resulted in a decrease in muscle glycogen and increase in muscle lactate levels (Fig. 3A,B). The decrease in glycogen and increase in lactate levels were equivalent in all groups. In control fish, muscle lactate levels did not show any signs of decline until 4 h post-exercise (Fig. 3B), at which time there was evidence of net glycogen synthesis (Fig. 3A). However, glycogen restoration and lactate clearance were still incomplete in control fish at 4 h. In contrast, in metyrapone-treated fish, muscle glycogen levels were completely restored within 2 h post-exercise (Fig. 3A), and this was associated with clearance of the lactate load to pre-exercise levels (Fig. 3B). Restoration of muscle glycogen and clearance of muscle lactate levels were delayed in the cortisol-treated group; there was no glycogen synthesis or clearance of lactate by 4 h after exercise in these fish (Fig. 3A,B).
|
At rest the maximum total activity of muscle glycogen phosphorylase (Phos)
was 0.63±0.08 U g wet tissue1 (N=8) that of
glycogen synthase (GSase) was 1.06±0.11 g wet tissue1
(N=8). The total activities of these enzymes did not change with
exercise, metyrapone or cortisol treatment. Instead, the relative activities
of the active form of the enzymes (Phos a and GSase I)
changed with exercise; the rate and direction of change were dependent upon
the cortisol level (Fig. 4A,B).
Phos a activity increased from 0.12 g wet tissue1
(N=8) at rest to 0.54 g wet tissue1 (N=8),
attaining approximately 85% of maximal activity immediately after exercise
(Fig. 4A). In control fish,
Phos a activity declined slowly, attaining pre-exercise levels by 4 h
post-exercise. However, in metyrapone-treated fish, Phos a activity
declined rapidly, returning to pre-exercise levels within 1 h of exercise,
whereas Phos a activity remained elevated throughout the 4 h period
in the cortisol-treated fish (Fig.
4A). GSase I activity was slow to increase in the control
group; it was not until 2 h post-exercise that evidence of activation was
seen, with activity further increased at 4 h, coincident with the time-frame
of glycogen synthesis (Fig.
3A). Significant increases in GSase I activity were seen
as early as 1 h post-exercise in metyrapone-treated fish, with peak activation
[0.59± 0.11 g wet tissue1 (N=8),55% of
total activity] seen at 2 h post-exercise. Again, these changes in GSase
I activity were coincident with glycogen resynthesis
(Fig. 3A). The activation of
GSase I in cortisol-treated fish was similar to that seen in the
controls (Fig. 4B), yet there
was no net glycogen synthesis in this group
(Fig. 3A).
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Muscle free glucose concentration increased late (24 h) into the post-exercise period in the control and cortisol-treated fish (Fig. 5A), but there was no change in glucose concentration in the metyrapone-treated fish. Muscle glucose-6-phosphate concentration increased immediately after exercise in the control and cortisol-treated groups and remained elevated throughout the 4 h post-exercise period. No change in glucose-6-phosphate concentration was seen in the metyrapone-treated fish (Fig. 5B).
|
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Discussion |
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Regulation of muscle glycogen metabolism in fish is not well understood
but, at least for glycogenolysis, seems to be similar to that described for
other vertebrates. The two most important stimuli of muscle glycogen breakdown
are contractile activity and increased circulating adrenaline levels
(Jensen et al., 1999).
Contractile-induced increases in intracellular [Ca2+] activate
phosphorylase kinase, which in turn, stimulates glycogen phosphorylase
activity and glycogenolysis (Yamamoto,
1968
). Adrenaline stimulates glycogen phosphorylase activity and
glycogenolysis via ß-adrenergic receptors, linked to the cAMP
signaling cascade (Jensen et al.,
1999
). A similar scenario probably occurs in trout, as adrenaline
infusion into resting catfish and trout stimulates glycogen phosphorylase
activity and glycogenolysis in white muscle
(Ottolenghi et al., 1984
;
Frolow, 1999
). This effect is
probably mediated by cAMP-linked ß-adrenergic receptors, which have
recently been identified in trout white muscle
(Lortie and Moon, 2003
).
The exercise-induced increases in levels of adrenaline, noradrenaline and
intracellular [Ca2+] were all probably important to the initial
stimulation of Phos a and resultant glycogen breakdown. By 2 h into
the recovery period, however, circulating catecholamine levels had decreased
in all experimental groups, but only in the control and metyrapone-treated
fish did Phos a activity decline; it was persistently elevated in the
cortisol-treated fish. Cortisol can exert a permissive effect on the actions
of catecholamines, such that the adrenergic response is enhanced by
glucocorticoids (e.g. Reid et al.,
1992). In trout this effect is seen in liver after chronic
(811 days) elevation of cortisol levels, and was associated with an
increase in adrenergic receptor density
(Reid et al., 1992
). Given the
short-term elevation of cortisol levels in this study (13 h vs
811 days), it is unlikely that the persistent elevation of Phos
a in the cortisol-treated fish was the result of a permissive effect
on adrenergic signaling. Furthermore, the fact that GSase I activity
was increased in the cortisol-treated group also argues against any permissive
effect on adrenergically mediated signaling, since catecholamines inhibit
GSase activity (e.g. Moon et al.,
1999
). Instead, the persistent elevation of cortisol levels was
likely to have been the cause of the continuous stimulation of Phos a
activity in the cortisol-treated fish. Trout muscle does contain
corticosteroid receptors, albeit at relatively low density compared to liver
or gill (Chakraborti et al.,
1987
; Ducouret,
1996
). While there is no evidence for any direct effects of
cortisol on fish muscle glycogen metabolism, dexamethasone (a glucocorticoid
analog) increases the activities of both Phos a and GSase I
in rat hepatocyte primary culture, and stimulates glycogenolysis. These
effects are independent of changes in the levels of Phos or GSase mRNA or
protein synthesis, but dependent upon extracellular [Ca2+],
suggesting glucocorticoids may activate Phos and GSase by modifying their
phosphorylation state (Baqué et al.,
1986
; Gomez-Muñoz et
al., 1989
). Current hypotheses are that glucocorticoids initiate
rapid signaling via nongenomic mechanisms, though whether
membrane-initiated steroid signaling is the proximate cause remains to be seen
(for reviews, see Falkenstein et al.,
2000
; Lösel and Wehling,
2003
). The mechanism by which glucocorticoids activate Phos in
trout muscle is highly speculative, but is likely to involve maintenance of
the phosphorylation state of Phos, rather than activation via
alteration of allosteric modifiers or substrates. The method used in this
study to assay Phos a activity only detects changes in activity due
to covalent modification, not any due to allosteric modifiers or substrate
concentration, because the enzyme activity is measured in a highly diluted
homogenate. The increase in GSase I activity may be a consequence of
elevated levels of glucose-6-phosphate, which can stimulate the
interconversion of GSase D to GSase I by increasing the
sensitivity of GSase D to phosphatases
(Villar-Palasi, 1991
;
Villar-Palasi and Guinovart,
1997
). Also, reduced glycogen levels themselves can lead to
dephosphorylation of GSase D, converting it to GSase I. In
various mammalian muscles, low glycogen levels are known to activate
phosphatases and inhibit phosphorylase kinase, and thus reduce Phos a
activity while stimulating that of GSase I
(Alonso et al., 1995
;
Laurent et al., 2000
). Whether
a similar mechanism is operating in fish muscle remains to be seen, but that
fact that there was no change in total activity of either Phos or Gsase in our
studies, suggests there was no de novo synthesis of these enzymes in
response to cortisol treatment.
As a consequence of the dual activation of Phos a and GSase
I, there is no net glycogen synthesis, suggesting that cortisol may
be stimulating glycogen cycling in the muscle. This certainly explains why the
persistent elevation of cortisol after exercise inhibits net glycogen
synthesis in trout (e.g. Pagnotta et al.,
1994; Eros and Milligan,
1996
; Milligan et al.,
2000
). The physiological significance of such a response, however,
is less clear. One hypothesis suggests that since muscle glycogenolysis
results in lactate production and cortisol stimulates hepatic lactate
gluconeogenesis, stimulation of glycogenolysis in muscle may provide lactate
for hepatic gluconeogenesis (see Mommsen
et al., 1999
). While lactate certainly accumulates in fish muscle
after exercise (see Fig. 3B), the vast majority of it stays there (see
Sharpe and Milligan, 2003
),
making it unavailable as a gluconeogenic substrate for other tissues. Rather,
the effect of cortisol on Phos a in muscle may reflect its general
role as an energy mobilizing hormone, keeping the muscle `primed' for rapid
energy mobilization via glycogenolysis. The simultaneous stimulation
of GSase could have been an indirect consequence of the cortisol-mediated Phos
a activation, which caused an increase in glucose-6-phophate and
decrease in glycogen levels, thus further stimulating GSase I
activity.
In summary, this study is the first report of an effect of cortisol on
muscle glycogen metabolism in fish. Further, these results provide a working
model to explain why cortisol elevation post-exercise is inhibitory to muscle
glycogen synthesis. The stimulation of Phos a and GSase I
activities in the absence of any change in total enzyme activity, in
conjunction with the relatively short time frame of action (1 h), suggest
that cortisol may be exerting its effects on muscle glycogen metabolism
via nongenomic action. Delineation of the interactions of cortisol
and fish muscle metabolism should prove a fruitful line of inquiry because
since the muscle constitutes such a large portion of the whole body mass, even
small metabolic changes may have a very large impact on the whole animal.
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Acknowledgments |
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